Life history of the bridge spider,
Larinioides sclopetarius (Clerck, 1757)
Dissertation
zur Erlangung des Doktorgrades
der Naturwissenschaften (Dr. rer. nat.)
dem Department Biologie der Fakultät für
Mathematik, Informatik und Naturwissenschaften
an der Universität Hamburg
vorgelegt von
Anja Kleinteich (geb. Nioduschewski)
geboren in Dinslaken
Hamburg im November 2009
Genehmigt
vomDepartment
Biologie
der Fakultätfür Mathematik,
Informatik
undNaturwissenschaften
an dqr Universität
Hamburg
aufAntragvon FrauProfessor
Dr.J. SCHNEIDER
WeitereGutachterin
der Dissertation:
FrauProfessor
Dr.M. E. HERBERSTEIN
Tagder Disputation:
18.Dezember
2009
Hamburg,
den27. November
2009
I {^,k
Professor
Dr.JörgGanzhorn
LeiterdesDepartments
Biologie
16 Nov 2009
Bestätigung der sprachlichen Korrektheit
Die sprachliche Korrektheit der in englischer Sprache abgefassten Dissertation von Frau Anja
Kleinteich (geb. Nioduschewski) mit dem Titel „Life history of the bridge spider, Larinioides
sclopetarius (Clerck, 1757)“ wurde von dem Unterzeichnenden, Dr. Mason N. Dean, geprüft und
bestätigt.
Sincer
rel
ely,
y
Sincerely,
Dr. Mason N. Dean
[email protected]
Table of contents
Zusammenfassung
7
Summary
9
General introduction
11
Chapter 1:
17
Developmental strategies in an invasive spider: constraints and plasticity
Chapter 2:
47
Evidence for Rensch’s rule in an orb-web spider with moderate sexual size
dimorphism
Chapter 3:
69
Dietary restriction increases lifetime fecundity and extends lifespan in a spider
General discussion
91
Danksagung
99
Zusammenfassung
Das Leben eines Organismus’ wird durch das Erreichen der Geschlechtsreife in zwei Phasen geteilt:
die Entwicklungs- und die Fortpflanzungsphase. Die Ausprägung der life history Parameter
(Schlupf- oder Geburtsgröße, Wachstumsmuster, Alter und Größe zur Reife, Anzahl, Größe und
Geschlechterverhältnis der Nachkommen, Fortpflanzungskosten, alters- und größenabhängige
Mortalität und die Lebensdauer) wird durch intrinsische (physiologische und genetische) und
extrinsische (ökologische) Faktoren bestimmt. Plastizität in life history Parametern ermöglicht
Arten, sich schnell an neue Umwelten, wie zum Beispiel urbane Habitate, anzupassen.
Die
Brückenspinne Larinioides sclopetarius ist extrem erfolgreich beim Kolonisieren von Städten
weltweit und bewohnt in großer Anzahl anthropogene Strukturen in Gewässernähe. Sie frisst
Insekten, die aus dem Wasser schlüpfen und von künstlichem Licht angelockt werden, in dessen
Nähe die Spinnen ihre Netze bauen. In Städten ist die Beuteverfügbarkeit sehr hoch, obwohl sie
zeitlichen und räumlichen Schwankungen unterliegt. Veränderungen in der Beutedichte können –
abhängig davon in welcher Lebensphase sie stattfinden – unterschiedliche Effekte auf die life
history Parameter haben. Diese Arbeit beschreibt den Einfluss der Nahrungsverfügbarkeit während
des gesamten Lebens (Entwicklungs- und Fortpflanzungsphase) auf die wesentlichen life history
Parameter von L. sclopetarius untersucht. Ziel war es, die verantwortlichen Parameter für den
Besiedelungserfolg der Brückenspinnen aufzudecken.
Sowohl die Weibchen als auch die Männchen zeigen abhängig von der Nahrungsverfügbarkeit
ein hohes Maß an Plastizität in allen Entwicklungsparametern, d.h. in der Anzahl der
Entwicklungsstadien, der Intervalle zwischen den Entwicklungsstadien und der Wachstumsrate.
Nahungsbeschränkungen verursachen bei beiden Geschlechtern zusätzliche Häutungen und eine
verlängerte Entwicklungszeit. Das Wachstum von Brückenspinnen folgt einem geometrischen
Verlauf und kann daher unter konstanten Umweltbedingungen gut prognostiziert werden.
Dennoch ist das Wachstumsverhältnis (Größenzuwachs pro Häutung) zwischen Häutungen nicht
konstant, was zu einer Abweichung von der Dyarschen Regel führt, welche konstante
Wachstumsverhältnisse zwischen Arthropoden-Häutungen postuliert.
L. sclopetarius zeigte in Bezug auf die Nahrungsverfügbarkeit während der Entwicklung auch
Unterschiede in den life history Parametern Größe, Gewicht und Alter zur Geschlechtsreife. Hohe
Futtermengen verursachten eine kürzere Entwicklungszeit, eine größere Adultgröße und ein
höheres Adultgewicht. Männchen und Weibchen unterliegen verschiedenen Selektionsdrücken
(Fekunditätsselektion
vs.
sexueller
Selektion),
was
gewöhnlich
zu
einem
Geschlechtsgrößendimorphismus führt (SSD = sexual size dimorphism). Die unterschiedlichen
7
ZUSAMMENFASSUNG
LIFE HISTORY OF THE BRIDGE SPIDER
Selektionsdrücke verursachen einen geringen männchengerichteten SSD (Männchen sind größer
als Weibchen) bei Brückenspinnen, wobei die Weibchengröße unabhängig vom Futterlevel und
daher kanalisiert (fixiert) war. Die größere Variabilität in der Männchengröße als in der
Weibchengröße entspricht der Renschschen Regel, was im Gegensatz zu anderen Studien an
Spinnen mit größerem SSD steht. Diese Studie ist die erste, die die Renschsche Regel in
Kombination mit männchengerichtetem SSD für Spinnen bestätigt.
Die Schlüsselparameter Größe, Gewicht und Alter zur Geschlechtsreife sind aufgrund ihrer
Bedeutung für Reproduktion und Überleben in hohem Maße fitnessrelevant. Um zu testen, wie
Nahrungsverfügbarkeit während des Wachstums und die life history Parameter den
Reproduktionserfolg beeinflussen, habe ich Brückenspinnenweibchen verpaart und sie während
ihrer Fortpflanzungsphase bis zu ihrem Tod beobachtet. Zusätzlich kontrollierte und veränderte ich
während dieser Phase die Futterbedingungen, um Auswirkungen der Nahrungsverfügbarkeit auf
die Anzahl ihrer Nachkommen zu analysieren. Männliche Brückenspinnen geben nach der
Adulthäutung den Bau von Radnetzen auf, so dass eine weitere Beeinflussung durch die Nahrung
nicht mehr durchgeführt werden konnte. Weibchen, die unter hoher Futterdichte aufwuchsen,
hatten eine erhöhte Fekundität und eine verlängerte Reproduktionsphase. Dennoch hat die
Futterverfügbarkeit nach der Adulthäutung einen größeren Einfluss auf die Reproduktionsrate als
die Futterverfügbarkeit während der Entwicklung. Hohe Futterverfügbarkeit während der
Fortpflanzungszeit führt zu einer höheren Nachkommenszahl und kürzeren Intervallen zwischen
den Gelegen. Weibchen, die in ihrem Leben wenig Futter zur Verfügung hatten, können die
Nachteile durch ihre verzögerte Entwicklung teilweise kompensieren indem sie ihren
Alterungsprozess (die Seneszenz) verlangsamen; sie können aber nicht so viele Nachkommen
zeugen wie Weibchen, denen viel Nahrung zur Verfügung stand. Überraschenderweise konnte ich
keinen Zusammenhang zwischen dem Eigewicht und der Nahrungsverfügbarkeit während des
Lebens finden, was vermuten lässt, dass die Nahrungsmenge nur einen Einfluss auf die Quantität
nicht aber auf die Qualität der Nachkommen hat.
Das Vorhandensein von großer Plastizität mit beschleunigtem Wachstum, die extreme
Variabilität in den life history Parametern und die unmittelbare Reaktion auf die
Nahrungsverfügbarkeit durch direkte Erhöhung des Reproduktionserfolges machen die
Brückenspinnen L. sclopetarius zu einem extrem erfolgreichen Besiedler urbaner Habitate und
demzufolge zu einem wichtigen Modell für Studien der Stadtökologie.
8
Summary
The life history of an organism is divided into two life stages termed developmental and
reproductive period that are separated by maturation. The shape of life history traits (size
at birth, growth pattern, age and size at maturity, number, size, and sex ratio of offspring,
reproductive investments, age- and size-specific mortality schedules, and length of life) is
determined by intrinsic (i.e. physiological and genetic) and extrinsic (i.e. environmental)
factors. The plasticity in life history traits influences the ability of a species to quickly adapt
to novel environments, such as urban habitats. The bridge spider Larinioides sclopetarius is
an extremely successful colonizer of cities worldwide and inhabits buildings near water in
huge numbers. The spiders feed on insects that emerge from the water and are attracted
to artificial lights, where the spiders build their webs. Prey availability is high in this habitat
although prone to spatial and temporal variation. Changes in prey abundance will have
differential effects on life history traits, depending on the life stage they are acting on. In
this thesis, I investigate the impact of food availability during the entire life (i.e.
developmental plus reproductive period) on the major life history parameters of L.
sclopetarius. Goal of this enterprise was to reveal the traits responsible for the invasiveness
of bridge spiders.
All developmental parameters such as the number of instars, the interval between
instars, and the growth rate showed a high degree of plasticity depending on diet in males
and females. Dietary restriction caused additional molts and a prolonged developmental
time in both sexes. The growth trajectory of bridge spiders followed a geometric
progression and was thus highly predictable under constant environments. However, the
growth ratios (size/weight gain per molt) were not constant, which is contrary to Dyar’s
rule that postulates constant growth ratios for successive instars in arthropods.
In relation to diet during development, L. sclopetarius further showed variability in the
life history traits size, weight, and age at maturity. High feeding conditions caused a
shorter development time and a larger adult weight and size. The sexes underlie different
selection pressures (fecundity selection vs. sexual selection), which usually result in a
sexual size dimorphism (SSD). In bridge spiders, these different selection pressures cause a
weak male-biased SSD and female size at maturity was independent of feeding level and
thus canalized. The higher variability in male body size than in female body size is in
9
SUMMARY
LIFE HISTORY OF THE BRIDGE SPIDER
accordance with Rensch’s rule, a finding that contrasts other growth studies in spiders with
more pronounced SSD. This study is the first to validate Rensch’s rule in combination with
male-biased SSD for the taxon.
The key life history parameters size, weight, and age at maturity are highly fitness
relevant due to their effects on reproduction and survival. To test how reproductive output
is influenced by food availability during growth and life history traits, I mated female
bridge spiders and followed them individually during their reproductive period until
death. Feeding conditions also were altered during the reproductive period, to study
proximate effects of diet on number of offspring. Male reproductive success was not
considered because they stop building orb-webs after maturation and thus can no longer
be influenced by variable diets. Females that grew under a rich diet had increased lifetime
fecundity and a prolonged reproductive period. However, compared to the impact of diet
during development, feeding condition after maturation had a more substantial impact on
current reproduction. A rich diet during the reproductive period lead to higher offspring
number and shorter intervals between successive clutches. Females that encountered
limited food availability throughout their lives partly compensate disadvantages caused by
delayed maturation and by slowing down senescence but they never produced offspring
numbers comparable to females on a rich diet. Surprisingly, I found no link between
lifetime diet and egg weight, suggesting an effect of food only on offspring quantity but
not quality.
The high developmental plasticity with accelerated growth, the extreme variability in
key life history parameters, and the immediate reaction to diet by current reproductive
output makes the bridge spider L. sclopetarius an extremely successful invader in urban
habitats and thus an important model in studies of urban ecology.
10
General introduction
The term 'life history' encompasses the lifecycles of organisms by characterizing their
variability in the principal' traits such as (1) size at birth, (2) growth pattern, (3) age and size
at maturity, (4) number, size, and sex ratio of offspring, (5) reproductive investments, (6)
age- and size-specific mortality schedules, and (7) length of life (Stearns 1992). The lifespan
of an organism and the related life history parameters are divided into the developmental
and reproductive period that starts with sexual maturation. In invertebrates such as
spiders, maturation is a distinct transition that not only affects the gonads but many other
traits as well. Some life history traits are mostly influenced by events during the
developmental period (so before maturation), others are exclusively influenced by events
after maturation, while others yet, seem to be the result of events during both phases. For
example, size at birth, growth pattern, and age and size at maturity are under the influence
of events during development. Offspring number and reproductive investment are mostly
dependent on events during the reproductive period while mortality and longevity are
relevant during both, developmental and reproductive periods.
Life history research identifies the role of natural selection in different organisms in
shaping traits that are beneficial for survival and reproductive success. Furthermore, by
studying life history traits we can explain other biological patterns, such as phenotypic
plasticity or sexual size dimorphism (Blanckenhorn 1998, Nylin and Gotthard 1998, Prenter
et al. 1999, Blanckenhorn et al. 2007).
Life histories are shaped by intrinsic and extrinsic factors. Intrinsic factors include the
genotype and trade-offs between life history traits, as a benefit for one trait often comes at
the cost of another. Extrinsic factors are ecological impacts on survival and reproduction
and comprise environmental factors such as food availability, population density, and
temperature (Stearns 2000). For example, temperature is known to accelerate growth in
ectothermal organisms (Atkinson 1994) and thus reduces the age at maturity. Similarly, an
increased diet generally increases the size and weight at maturity (Roff 1992, Blanckenhorn
1998, Mayntz et al. 2003, Uhl et al. 2004, Marczak and Richardson 2008) and will also
directly influence the quantity and/or quality of offspring (Wise 1979, Sota 1985, Parker
and Begon 1986, Pékar 2000, Agarwala et al. 2008).
11
GENERAL INTRODUCTION
LIFE HISTORY OF THE BRIDGE SPIDER
This thesis investigates the influences of intrinsic and extrinsic factors during
development and reproduction on life history traits in an orb-web spider. The bridge
spider, Larinioides sclopetarius (Araneae, Araneidae), is a synanthropic nocturnal orb-web
spider with a holarctic distribution and can be overabundant along waterfronts in urban
habitats (Burgess and Uetz 1982, Heiling 1999, Schmitt 2004, Schmitt and Nioduschewski
2007a, Schmitt and Nioduschewski 2007b). Their high population densities (up to 100
individuals per m2, Nioduschewski and Kraayvanger 2005) on artificial structures (e.g.
bridges, facades) and their waste (i.e. webs, droppings, exuviae) makes them a nuisance for
inhabitants of buildings near water. Their presence can result in economic loss, especially
in residential and office districts close to the waterfront.
Habitats that are occupied by bridge spiders often have no other orb-web spiders
present (pers. observation). Other spiders are either completely outcompeted or are
restricted to occasional patches with low population densities (e.g. Zygiella x-notata,
Araneus diadematus). Although bridge spiders are ecologically and economically important
in urban habitats, the biological base for their success is poorly known.
An explanation of the high densities of bridge spider population in urban habitat is the
superabundance of prey associated with water. Illuminated structures and artificial light
sources in urban habitats attract insects with positive phototaxis (Wigglesworth 1942).
These insects are an enormous food resource for nocturnal predators such as bridge
spiders. Along waterfronts of urban habitats, most of the insects attracted by light emerge
from water dwelling larvae (e.g. Chironomidae, Oliver 1971). However, insect densities
fluctuate throughout the season (Ziegler 2005) and periods of overabundance of prey
items are followed by periods with less food. Thus it is likely that bridge spiders have
evolved different life history strategies to respond to such fluctuations. To investigate the
effects of different prey abundances on their life history, I reared L. sclopetarius under
controlled laboratory conditions from birth until death and documented the impact of
feeding conditions on the life stages development, maturation, and reproduction. The
single Chapters of this thesis consider these three different life stages.
Chapter 1 focuses on the development of bridge spiders and considers their growth
patterns and developmental plasticity. The development of arthropods can be described
by three developmental parameters that determine the life history traits size, weight, and
age at maturity: (1) number of instars (i.e. developmental stages), (2) intervals between
12
LIFE HISTORY OF THE BRIDGE SPIDER
GENERAL INTRODUCTION
instars, and (3) size/weight gain per molt. In response to variable environmental
conditions, in arthropods at least two of the three developmental parameters are plastic
(flexible) (Higgins and Rankin 1996). Many arthropods follow geometric growth rules that
are described by a constant growth ratio (i.e. size/weight gain per molt) (Dyar 1890,
Przibram and Megušar 1912, Hutchinson et al. 1997). The existence of constant growth
ratios is contrasted by developmental plasticity and geometric growth progressions are
likely to constrain the plastic responses to variable environmental conditions. Chapter 1
integrates developmental plasticity, growth patterns, and invasiveness in urban habitats.
Chapter 2 describes the plasticity and sex specific differences of the major life history
traits size, weight, and age at maturity. These major traits are linked by trade-offs and are
under the influence of three levels of selection (i.e. fecundity, sexual, and viability
selection) that act differentially on males and females (Blanckenhorn 2000, Blanckenhorn
et al. 2007). The sex specific selection pressures on life history traits often result in sexual
size dimorphism (Blanckenhorn 2000, Blanckenhorn et al. 2007) with male size usually
being more variable than female size (Rensch’s rule, Rensch 1950, Fairbairn and Preziosi
1994, Fairbairn 2005, Blanckenhorn et al. 2007). Chapter 2 discusses the different selection
pressures on life history traits and sexes, the trade-offs between those traits, and
phenotypic effects such as sexual size dimorphism and Rensch’s rule in L. sclopetarius.
Chapter 3 investigates the reproductive success (i.e. lifetime fecundity) of female bridge
spiders and its relation to the diet at different life stages and lifespan. Lifetime fecundity in
arthropods is often positively related to female body size (Wickman and Karlsson 1989,
Honek 1993, Marshall and Gittleman 1994, Head 1995, Foellmer and Moya-Laraño 2007)
and to feeding condition (Wise 1979, Sota 1985, Parker and Begon 1986, Pékar 2000,
Agarwala et al. 2008). Under poor diet, animals extend their lifespan (Masoro 2005) and
thus prolong the reproductive period. In Chapter 3, I investigate the trade-off between
lifespan and offspring number in bridge spiders to reveal the reproductive strategies that
are the basis for their success in urban habitats.
13
GENERAL INTRODUCTION
LIFE HISTORY OF THE BRIDGE SPIDER
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LIFE HISTORY OF THE BRIDGE SPIDER
GENERAL INTRODUCTION
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LIFE HISTORY OF THE BRIDGE SPIDER
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16
Chapter 1
Developmental strategies in an invasive spider:
constraints and plasticity
Abstract Growth defines the major life history traits such as size, weight, and age at
maturity that determine an organism’s fitness. Different models have been developed to
describe growth by means of geometric progressions (e.g. Dyar’s rule). However, growth
along a geometric trajectory seems to be in contrast with developmental plasticity that is a
common phenomenon in response to variable environmental conditions (e.g. food
availability). We investigated growth patterns under varying food conditions in the bridge
spider, Larinioides sclopetarius, an extremely successful species in colonizing urban
habitats. Growth of L. sclopetarius does not follow Dyar’s rule because growth ratios
decreased over development. Nevertheless, growth can be described by geometric
progressions that comprise a growth factor (weight gain per molt) and a growth
coefficient (weight gain per development time). In Larinioides sclopetarius, all
developmental parameters, including growth factor and growth coefficient as well as the
intermolt duration and the number of instars, highly depend on food availability and show
full plasticity. This study shows that plasticity does not necessarily preclude geometric
growth patterns. However, the parameters of geometric growth are affected by
developmental plasticity. Our study provides evidence that the ability of bridge spiders to
successfully invade urban habitats is related to their high developmental plasticity.
17
CHAPTER 1
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
Introduction
Adult fitness of any organism is to a large extent the result of life history strategies during
development; juvenile growth is one of the principal life history traits. Growth determines
size and age at maturity and often reproductive fitness (Stearns and Koella 1986, Vollrath
1987, Roff 1992, Stearns 1992). Growth itself is a function of environmental conditions in
concert with the genetic disposition.
The ability to react adaptively to changing environmental conditions will define the
trajectory between juvenile growth and adult fitness (Abrams et al. 1996). Growth patterns
of animals are categorized into two separate dichotomies as determinate vs.
indeterminate, continuous vs. discontinuous growth. Determinate growth stops at some
point in life (e.g. certain size or age, usually after reaching sexual maturity) and
indeterminate growth continuous as long as the animal survives (Karkach 2006).
Discontinuous growth describes the stepwise growth of arthropods as well as the so-called
“catch-up” growth of animals with a genetically determined final size (e.g. clams in the gulf
of California) (Karkach 2006). In the latter example, individuals with slow growth early in
life due to poor conditions will catch up if conditions improve. Continuous growth cannot
be divided into discrete stages.
The main growth categories described above can be further divided into distinct
developmental categories. Animals with metamorphosis go through a biphasic
development (e.g. amphibians, holometabolous insects), while others develop directly
(e.g. mammals, hemimetabolous insects). A biphasic development always includes a larval
stage, a metamorphosis and an adult stage (Zissler 2003).
In contrast to indeterminate and continuous growth, determinate growth of
hemimetabolous arthropods is characterized by consecutive stages each of which may
have growth rates independent of other stages. Arthropods grow discontinuously due to
their cuticle that prevents the exoskeleton from expanding outside molts. Theoretically,
hemimetabolous growth may allow an animal to repeatedly adjust current growth
decisions to prevailing conditions until maturation. Such a flexibility is known for
insectivorous
arthropods,
while
in
many
phytophagous
(hemimetabolous
or
holometabolous) insects the flexibility to react to local conditions is restricted to the very
beginning of their life (Nijhout and Williams 1974, Hatle et al. 2003).
18
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
CHAPTER 1
In an attempt to explain the variability in arthropod growth patterns, Higgins and
Rankin (1996) postulate that 1) three developmental parameters (change in size at ecdysis,
intermolt duration, number of instars) determine age and size at maturity, but 2) never
more than one is fixed (canalized), and 3) not all combinations of plastic (flexible) and
canalized parameters occur in nature. Plasticity is the flexibility of an organism to react to
internal or external environmental factors with a change in form, state, movement, or rate
of activity (West-Eberhard 2003); canalization is the opposite. Canalization describes a
genetic fixation of traits resulting in expression of the same phenotype regardless of
environmental variation (Nylin and Gotthard 1998). However, most life history traits show
phenotypic plasticity in response to changing environmental factors during development
(Caswell 1983).
The potential to modulate growth adaptively is contrasted by the idea of growth rules,
which postulate that animals can only grow at a distinct and constant ratio. Dyar (1890)
proposed that arthropods grow with a regular geometrical progression a pattern known as
Dyar’s rule. Later Przibram and Megušar (1912) determined the growth ratio (i.e. the size of
one instar divided by the size of the preceding instar) to be 1.26. Cole (1980) listed
additional growth ratios for 105 insect species. Comparable to Dyar’s rule for the increase
of body size, Przibram and Megušar (1912) found a geometric progression for the weight
increase of successive instars (by a factor of two).
The existence of a fixed growth factor implies that all individuals of a holometabolous or
hemimetabolous arthropod species reach the same size at maturation unless the number
of instars varies. The number of instars or molts determines in how many steps an
individual reaches maturity and gains weight. However, growth of arthropods is also
determined by intermolt intervals that determine the time an animal takes to gain weight
between molts.
Empirical results are ambiguous although most studies support Dyar’s ideas (Moser et
al. 1991, Alvan-Aguilar and Hamada 2003, Fusco et al. 2004, Hernandez-Livera et al. 2005,
Massuretti de Jesus and Correa Bueno 2007, Panzavolta 2007, Rodriguez-Loeches and
Barro 2008). Some insect species, however, are reported to follow Dyar’s rule in only some
of their instars (Lauzon and Harper 1993), in only some morphological structures (Johnson
and Williamson 2006), or in particular caste stages of social insects (Cnaani and Hefetz
2001). Other studies did not find constant growth rates between growth stages
19
CHAPTER 1
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
(Klingenberg and Zimmermann 1992, Tomkins 1999, Calvo and Molina 2008) due to the
effects of environmental changes such as crowding, temperature, and food availability
(Daly 1985, Hutchinson et al. 1997, Mayntz et al. 2003, Guillen and Heraty 2004).
Spiders generally show a hemimetabolous, determinate growth, which is proposed to
critically depend on food availability. In particular, spider species that are sit-and-wait
predators depend on prey abundance due to their limited impact on numbers and kinds of
prey (Mayntz et al. 2003). They can only influence their prey capture success by choosing
web position, changing web size, or by varying mesh size (Olive 1982, Herberstein and
Elgar 1994, Sherman 1994, Heiling and Herberstein 1998). As a consequence, sit-and-wait
predators are well adapted to variable prey availabilities (Mayntz et al. 2003). Dyar’s rule
has been applied to very few spider species and the results allow no confident conclusion
about its applicability. While an actively hunting wolfspider Pardosa astrigera (Lycosidae)
showed deviations from a constant growth factor (Miyashita 1968), the orb-web spider
Nephila clavipes (Nephilidae) exhibited fixed growth ratio between instars (Higgins 1992,
Higgins 1993, Higgins and Rankin 1996). Enders (1976) found deviations from constant
growth factors in several spider species of the families Salticidae and Lycosidae.
Dyar’s rule would be most effectively tested through examination of a species with a
particular advantage for developmental plasticity. In our study, we investigate growth
trajectories and patterns under varying environmental conditions in an invasive orb-web
spider, Larinioides sclopetarius (Araneidae). The bridge spider, L. sclopetarius, is extremely
successful in colonizing urban habitats. It is a synanthropic species that is very abundant
near water and considered a pest in large cities (Heiling 1999, Schmitt 2004, Schmitt and
Nioduschewski 2007). The spiders aggregate near water, a consequence of the
superabundance of insect prey that emerges from the water and is attracted of artificial
lights in manmade habitats (Burgess and Uetz 1982, Heiling 1999). As an invasive species,
L. sclopetarius is predicted to be particularly plastic because flexibility predisposes them to
quickly adapt to novel environments. To test this assumption, we raised spiders from eggs
and followed their growth until maturation while varying food supply across experimental
groups. We hypothesized that these spiders do not show constant growth ratios between
successive instars but display a high degree of plasticity in their growth factor (weight gain
per molt), the number of instars, and the aging factor (instead of intermolt duration) that
may allow them to be successful colonizers.
20
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
CHAPTER 1
Methods
Study objects
The bridge spider Larinioides sclopetarius (Clerck, 1757) (Araneae: Araneidae) is very
common in urban habitats. It is a nocturnal synanthropic species that is very abundant
near water and lives in aggregations. Under laboratory conditions females produce up to
15 cocoons over a lifespan of 1.5 years. All developmental stages are present throughout
the year, with adult males abundant mainly in September. Cocoons do not hibernate.
Individuals of the spider L. sclopetarius were collected from their webs on bridges and
facades in populations near the River Elbe in the HafenCity of Hamburg, Germany (53°33'N,
09°59'E), in 2006 from May to October and in April, 2007.
Parent generation
Spiderlings for experiments originated from 24 females; of these, 21 females were mated
with virgin males in the laboratory and three females mated in the field. From the 21
female specimens that were mated in the laboratory, seven were collected in the field in
the penultimate instar and 14 were derived from laboratory breeds. Altogether observed
offspring were derived from 15 maternal lines (cp. Table 8 appendix). In addition to
variation in locality and mating location, mothers differed in the duration between
maturation and mating. From each mother we chose a single cocoon from which offspring
were delivered for treatments (cp. Table 9 appendix).
Rearing conditions
Reproductive spiders were kept individually in 400 ml plastic cups at room temperature
and under natural photoperiod. Spiders were fed 2-3 blowflies (Calliphora sp.) twice a
week, and watered once per day, five days per week. After their final molts, females were
weighed and transferred to Perspex frames (36 × 36 × 6 cm) where they built their orb
webs. Females were mated 3-83 days (in average 42 days) following maturation. Males
were maintained in individual 200 ml plastic cups, fed 5-10 Drosophila melanogaster twice
a week, and watered five days per week. Mated females were transferred back to their
plastic cups and checked for egg sacs five days per week. Deposited egg sacs were
weighed, maintained in boxes (7 × 14.5 × 11.5 cm) and randomly assigned to three
21
CHAPTER 1
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
different temperatures – room temperature (20-25 °C), low temperature (20 °C) or high
temperature (30 °C) in an incubator (cp. Table 8 appendix) – and watered daily five times a
week.
Feeding treatments/Feeding experiments
Ten days after hatching, 15 full-sibling spiderlings were randomly assigned to three
different diet regimes: (i) high feeding level, (ii) low feeding level, or (iii) very low feeding
level. Due to the experimental design mothers that vary in locality, mating location, period
elapsing between maturation and mating, successive number of egg sac were represented
in all treatments. All juveniles were separated in the second instar because first molts occur
inside the egg sac about three days after hatching. The first weighing of spiderlings was
performed after the second molt. Animals in the high feeding treatment received
Drosophila melanogaster ad libitum. Drosophila melanogaster were fed on a high nutrient
diet with Carolina Biological Supply instant Drosophila medium Formula 4-24® and crushed
dog food (Purina Matzinger Flocken-Vollkost Junior) according to Mayntz and Toft (2001).
Food was limited in the low and very low feeding treatment. The first feeding was
performed fifteen days after hatching: spiders with low feeding level were fed three D.
melanogaster, very low feeding level spiders received one D. melanogaster per week (cp.
Table 7 appendix). With increasing age of spiders until maturation, we adjusted the
number of fed fruit flies every 60 days by a factor of 1.5-2.
Spiderlings were fed twice a week, watered and checked five days per week for the
presence of exuviae. Spiders were weighed after each molt (post-molt weight) using an
electronic balance (METTLER TOLEDO XS105 DualRange) to an accuracy of 0.01 mg. For
individuals on the high feeding treatment Drosophila were always available and therefore
we cannot exclude that they fed before post-molt weight was determined. From
September, 2006 to March, 2008 the development of 360 individuals (120 per treatment)
was observed. Of this group, 93 individuals died (for mortality see results) or were lost
during daily handling. The remaining 267 spiders reached adulthood, 138 females and 129
males. After death of adult spiders, the tibia-patella length of the first pair of legs was
measured to the nearest 0.01 mm using a LEICA MZ 16 stereomicroscope and LEICA IM500
imaging software (Version 4.0).
22
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
CHAPTER 1
In bridge spiders, sex cannot be assessed until the penultimate instar and so,
coincidentally in some cases, the siblings allocated to a particular treatment were the same
sex; as a result, some families are missing in some treatments. At the end of the study, the
developmental time from birth to adulthood, the number of instars, post-molt weight, and
inter-molt intervals of each individual were documented.
Developmental parameters
We examined the following developmental parameters: growth ratio, number of instars,
growth factor (weight gain per molt), aging factor (age gain per molt, instead of intermolt
interval), and growth coefficient (weight gain per development time).
The growth ratio of instar (ni) is defined as weight of current instar (ni) divided by weight
of the previous instar (ni-1). To exclude the possible effect of total number of instars on
growth ratio, we used only individuals with the same number of instars for the comparison
of growth ratios within the treatments. We started counting the number of instars
(developmental stages) beginning with their hatching out of the eggs; the first instar is
prior to the first molt.
To account for potentially different growth ratios between successive molts, we do not
use mean growth ratios of successive instars for the description of growth in different
treatments. To obtain values that are independent of the number of instars and describe
each treatment, we use an exponential growth equation:
yG  a  FG .
x
(1)
In this equation (1) yG is the post-molt weight, x is the number of molt, FG is the growth
factor, and a is a constant with no biological relevance, representing the value of y for x = 0.
The factor FG describes the weight gain per instar.
To consider the potential plasticity in the intermolt duration of successive instars, we
applied, an analogue to the growth factor, an aging factor FA that can be derived from the
exponential function:
y A  a  FA
x
(2)
In this equation (2) yA is the molting age, x is the number of molt, FA the aging factor, and a
is a constant. Rapid growth or aging is characterized by high values of FG or FA.
23
CHAPTER 1
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
To determine the values for FG and FA, we use the linear representation of the equations
(1) and (2):
ln(yG) = ln(a) + ln(FG) x
(3)
ln(yA) = ln(a) + ln(FA) x.
(4)
Linear regression of weight or age (ln(y)) over the number of molts (x) yields values for
ln(FG) and ln(FA) (i.e. the slope of the regression equation).
Post-molt weight over development time (independent of the number of instars) can be
generally described by the power function:
yG  a  xt ,
G
(5)
where yG is the weight, xt is the development time, a is a constant with no biological
relevance, representing the value of y when xt = 1, and G is the growth coefficient (based on
Huxleys (1950) growth rate). Rapid growth is characterized by high values of G. The linear
representation of equation (5) is:
ln(yG) = ln(a) + G ln(xt).
(6)
The value for G can be determined by linear regression of weight (ln(yG)) over development
time (ln(xt)) and resembles the slope of the regression equation.
Statistical analysis
We used the REML (Restricted Maximum Likelihood) method for fitting mixed model
ANOVAs (Analysis of Variance) to the data to estimate the effects of feeding treatment and
sex on the number of instars, the growth factor, the aging factor, and the growth
coefficient. Feeding treatment and sex were fixed factors and family was a random factor.
An exclusion of the family effect in the model does not alter results. Response variables
were transformed, if necessary. All residuals were normally distributed. Growth ratios and
intermolt durations over instars are not normally distributed. To estimate the effects of the
instar on the growth ratio and the intermolt duration we used the non-parametric
Friedman repeated measures analysis of variance on ranks. For individual pairwise
comparisons of least square means in the model we used Student’s t-test. In case more than
two parameters were present, we used the Tukey’s HSD (Honestly Significant Difference)
test to test all differences among the least square means. We used a chi-square
contingency analysis where mortality was the fixed factor and the treatment was the
24
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
CHAPTER 1
response. The statistical analyses were performed using JMP® 7.0.2 (SAS Institute Inc.) for
Microsoft® Windows. For models which are fitted with the REML method, JMP® does not
calculate F-ratios or P-values for the random factor family.
Results
The family significantly influenced the number of instars, the growth factor, the aging
factor and the growth coefficient (Table 1).
Table 1 Results of ANOVA for the effects of feeding level (treatment) and sex on number of instars,
growth factor (base FG in yG(weight)=a∙FGx(molt)), aging factor (base FA in yA(age)=a∙FAx(molt)), and
growth coefficient G (power of x in yG(weight)=a∙x(age)G) on spiderlings (N = 267).
number
of instars
growth
factor FG
ageing
factor FA X
growth
coefficient G X
variable
DF
F
p
F
p
F
p
F
p
treatment
2
103.75
<0.0001
213.06
<0.0001
114.28
<0.0001
287.49
<0.0001
sex
1
132.85
<0.0001
0.15
0.7023
10.73
0.0012
6.04
0.0146
sex ×
treatment
2
8.28
0.0003
3.75
0.0248
2.82
0.0614
1.47
0.2328
Number of instars
Bridge spider development was plastic in the total number of instars. The number of
instars depended on the feeding treatment and the sex. Females on average passed
through one more instar than males (Fig. 1, 2, Table 1). Males needed at least six and a
maximum of nine instars, females needed at least six but could take up to 10 instars (Table
2). The average number of instars of siblings within treatments was 6-9 for males and 7-10
for females (Fig. 2). With increasing food supply, both sexes required significantly fewer
molts to reach adulthood (Fig. 1, 2, 3, Table 1, 2).
25
CHAPTER 1
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
number of instars
9.5
growth factor
b
c
9.5
9.0
8.5
8.5
8.0
8.0
7.5
7.5
7.0
7.0
6.5
6.5
2.8
a
b
c
2.8
2.6
2.6
2.4
2.4
2.2
2.2
2.0
2.0
1.8
1.8
1.6
1.6
1.8
aging factor
a
9.0
a
b
c
1.8
1.7
1.7
1.6
1.6
1.5
1.5
1.4
1.4
1.3
1.3
1.2
1.2
high low very low
feeding level
a
b
a
a
a
b
females males
sex
Fig. 1 Box plots for comparison of various developmental parameters (number of instars, growth
factor, aging factor) of bridge spiders at different feeding levels (left) and sexes (right). Box plots
that are not connected by the same letter are significantly different. Feeding level and sex
influence all developmental parameters studied herein except for the growth factor, which is
independent of sex. All values for siblings within the same treatment or sex were averaged.
Growth ratio
The growth ratio describes the weight gain between successive instars and decreases with
increasing instar number in all food treatments except for those males under very low food
conditions (Fig. 4, Table 3). In all treatments and sexes that had a decrease in growth ratio,
at least the first and the last calculated growth ratios were significantly different (Fig. 4,
Table 3). Better feeding conditions (i.e. more frequent feedings) resulted in a more rapid
decrease of growth ratios of consecutive instars (Fig. 4). Mean values of growth ratios
within instars ranged from 2.93 (female high, instar IV) to 1.59 (female very low, instar IX).
26
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
CHAPTER 1
Table 2 Larinioides sclopetarius sample sizes and numbers of instars at different feeding levels.
Relative values in percent given in parenthesis. Bold values show highest percentages inside
treatments.
feeding level
♀
♂
N (%)
VI
high
low
very low
44 (100)
47 (100)
47 (100)
3 (6.8)
high
low
very low
51 (100)
49 (100)
29 (100)
4 (7.8)
N =
22
number of individuals with
VII
VIII
IX
instars
21
22
25 (56.8)
1 (2.1)
1 (2.1)
16 (36.4)
30 (63.8)
16 (34.0)
15 (31.9)
27 (57.4)
45 (88.2)
32 (65.3)
9 (31.0)
2 (3.9)
17 (34.7)
16 (55.2)
4 (13.8)
20
17
22
X
1 (2.1)
3 (6.4)
100%
80%
no. of instars
X
IX
VIII
VII
VI
60%
40%
20%
0%
high
low
females
very
low
high
low
very
low
feeding level
males
Fig. 2 Relative distribution of male and female spiders with n instars from hatching to adulthood at
high, low, and very low feeding level. Lower food availability increases the number of instars for
females and males. Average males have fewer instars than females in the same treatment. Females
underwent seven to ten instars, males six to nine. All values for siblings within the same treatment
and sex were averaged.
Growth factor
The growth factor FG is a single value that describes the general growth trajectory from
birth to maturation instead of using an averaged growth ratio for successive instars. A
large value for FG shows a rapid weight gain. Independent of sex, feeding treatments
showed significant differences in the growth factor (Fig. 1, Table 1). Individuals
experiencing high feeding conditions had the greatest weight increase over development
27
CHAPTER 1
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
(FG = 2.4); in the very low treatment the weight gain over development was lowest (FG =
1.9) (Table 5). The growth factor was not significantly different for males and females
(Table 1) with a mean value of 2.0 (Fig. 1). Different feeding levels showed significant
differences in growth factors for both males and females (Fig. 3). There was a significant
interaction between sex and treatment (Table 1) but the response in growth factors to
different treatments was the same for males and females (Fig. 3).
The relationship of post-molt weight over instar was well described by the exponential
function (1); its regression equation (4) for determination of FG yielded high correlation
coefficients (R2 > 0.99) (Table 5).
females
males
10
10
number of instars
a
growth factor
c
9
9
8
8
7
7
6
6
2.8
a
b
c
2.8
2.6
2.6
2.4
2.4
2.2
2.2
2.0
2.0
1.8
1.8
1.6
1.6
2.0
aging factor
b
a
b
c
2.0
1.8
1.8
1.6
1.6
1.4
1.4
1.2
high low very low
feeding level
1.2
a
b
c
a
b
c
a
b
b
high low very low
feeding level
Fig. 3 Box plots for comparison of various developmental parameters (number of instars, growth
factor, aging factor) at different feeding levels in female (left) and male (right) bridge spiders. Box
plots that are not connected by the same letter are significantly different. Feeding levels influence
all developmental parameters studied herein similarly for both sexes except for the aging factor of
males at low and very low feeding level. All values for siblings within the same treatment and sex
were averaged.
28
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
CHAPTER 1
males
females
4.0
a
a
ab
4.0
bc
3.5
3.5
3.0
3.0
high
2.5
y=2.95-0.2319x
1.0
growth ratio
a
a
ab
ab
4.0
bc
3.5
3.0
3.0
low
2.5
2.0
a
b
y=2.42-0.1195x
1.0
a
a
a
ab
a
4.0
bc
a
a
a
a
a
3.5
3.0
very
low
2.5
3.0
2.5
2.0
2.0
1.0
a
2.5
1.5
y=2.37-0.0946x
3.5
1.5
a
2.0
1.0
4.0
b
2.5
3.5
1.5
a
1.5
y=3.06-0.1921x
1.0
4.0
a
2.0
2.0
1.5
a
1.5
y=2.12-0.0627x
IV
V
VI
y=1.94-0.0004x
VII VIII
1.0
IX
IV
V
VI
VII VIII
IX
instar
instar
Fig. 4 Growth ratios (weight instar(ni)/weight instar(ni-1)) of successive instars in female (left) and
male (right) bridge spiders at high (top), low (middle), and very low (bottom) feeding levels. Instars
that are not connected by the same letter are significantly different. Growth ratios between molts
at the same feeding level are not constant and decrease except for the growth ratios of males at
very low feeding level. The negative slope of the linear regression decreases with declining feeding
level. (cp. Table 2 for sample sizes).
Table 3 Results of Friedman repeated measures analysis of variance on ranks for the effect of instars
on growth ratios (weight instar(ni)/weight instar(ni-1)).
total
number of
instars
♀
high
VII
low
VIII
very low
IX
feeding
level
♂
high
low
very low
VII
VII
VIII
DF
χ2
p
3
4
5
13.636 0.0003
10.993 0.0270
22.691 <0.0001
3
3
4
54.971 <0.0001
40.779 <0.0001
0.629
0.960
29
CHAPTER 1
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
Intermolt duration
The days between successive molts are considered as intermolt duration or intermolt
interval. Overall mean values for intermolt durations ranged from 8.2 days (female high,
instar IV) to 85.6 days (male very low, instar VII). Consecutive instars differed in their
intermolt duration in all treatments and both sexes (Fig. 5, Table 4). Intermolt duration
increased with successive instars (Fig. 5). Feeding levels affected intermolt duration; high
feeding conditions resulted in shortest intermolt durations.
females
140
a
ab
bc
males
140
c
120
120
100
100
80
intermolt duration [days]
40
20
20
0
0
a
a
a
bc
140
c
120
120
100
100
80
40
20
20
0
0
a
a
a
b
b
140
b
a
b
c
a
a
a
b
IV
V
b
120
120
100
100
very
low
80
60
80
60
40
40
20
20
0
a
60
40
140
b
80
low
60
b
60
40
140
a
80
high
60
a
IV
V
VI
VII VIII
IX
instar
0
VI
VII VIII
IX
instar
Fig. 5 Intermolt duration in days of successive instars in female (left) and male (right) bridge spiders
at high (top), low (middle), and very low (bottom) feeding level. Instars that are not connected by
the same letter are significantly different. Intermolt durations at the same feeding level are not
constant and increase (cp. Table 2 for sample sizes).
30
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
CHAPTER 1
Table 4 Results of Friedman repeated measures analysis of variance on ranks for the effect of instars
on intermolt duration.
total
number of
instars
♀
high
VII
low
VIII
very low
IX
feeding
level
♂
high
low
very low
VII
VII
VIII
DF
χ2
p
3
4
5
39.894
82.734
78.291
<0.0001
<0.0001
<0.0001
3
3
4
38.008
64.689
41.503
<0.0001
<0.0001
<0.0001
Table 5 Parameters of linear regression equation ln(yG) = ln(a) + ln(FG) x for the growth factor FG with
weight (y) over molt (x) and a as constant and Pearson correlation coefficient R2. FG values that are
not connected by the same letter are significantly different. All values for siblings within the same
treatment and sex were averaged.
feeding level
♀ high
low
very low
a
0.29
0.36
0.41
FG
2.42a
2.01bc
1.89d
R2
0.9951
0.9928
0.9957
♂
0.32
0.36
0.38
2.35a
2.06b
1.94cd
0.9934
0.9944
0.9944
high
low
very low
Table 6 Parameters of linear regression equation ln(yA) = ln(a) + ln(FA) x for the aging factor FA with
weight (y) over molt (x) and a as constant and Pearson correlation coefficient R2. FA values that are
not connected by the same letter are significantly different. All values for siblings within the same
treatment and sex were averaged.
feeding level
♀ high
low
very low
a
10.91
10.86
11.20
FA
1.35a
1.47b
1.56c
R2
0.9799
0.9865
0.9773
♂
11.23
9.33
10.05
1.36a
1.54c
1.63c
0.9784
0.9805
0.9865
high
low
very low
31
CHAPTER 1
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
Aging factor
The aging factor FA describes the aging over successive instars and is an alternative variable
to the mean value for intermolt durations. High values for FA represent long intermolt
durations. FA differed significantly in all treatments independent of sex (Table 1): under
high food, intermolt intervals were the shortest and spiders aged with a mean FA of 1.35.
The mean FA increased to 1.52 under low food and showed a further but slight increase
under very low food (1.58). Males aged with a slightly higher mean aging factor than
females (1.49 and 1.46, respectively). Feeding levels influenced the aging factors of males
and females significantly (Fig. 3, Table 1); males at low and very low feeding level showed
no significant differences in aging factors (Table 6). The relationship of age over instar was
well described by the exponential function (2); the correlation coefficient for the linear
regression that was used to determine FA exhibited values of R2 > 0.97 (Table 5).
Fig. 6 Mean growth curves of female and male bridge spiders as a function of different feeding
levels. Termination of each graph represents maturation. Individuals with high feeding level grow
in a shorter time to a larger weight than individuals with less food. Growth coefficients (cp. Table 6)
of different treatments are significantly different for both sexes (cp. Table 1). All values for siblings
within the same treatment and sex were averaged.
32
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
CHAPTER 1
Growth coefficient
The correlation between body weight and duration of development (Fig. 6) follows a
power function (5) with growth coefficient G as power. G describes the weight gain over
development time (days) independent of discrete instars. Large values for G depict a rapid
growth. Overall feeding treatment and sex affected the growth coefficient significantly but
there was no significant interaction between treatment and sex (Table 1). Individuals at
high feeding level had the highest growth coefficients and those at the very low feeding
level had the lowest. The growth coefficient differed significantly among feeding
treatments for males and females (Table 7). Independent of feeding conditions, males and
females shared the same mean growth coefficient of 2.07. The relationship of post-molt
weight over development time was well described by the power function (5); the linear
regression equation (6) that results in values for G had Pearson correlation coefficients of R2
> 0.97 (Table 7).
Table 7 Parameters of linear regression equation: ln(y) = ln(a) + G ln(x) with G as growth coefficient
and Pearson correlation coefficient R2. G values that are not connected by the same letter are
significantly different. All values for siblings within same treatment and sex were averaged.
feeding level
♀ high
low
very low
ln(a)
-8.30
-5.50
-4.24
G
2.96a
1.83b
1.41c
R2
0.9773
0.9837
0.9780
♂
-8.26
-4.72
-4.12
2.91a
1.65b
1.36c
0.9798
0.9765
0.9853
high
low
very low
Mortality
Out of 298 individuals, 10.4% died but there were no significant differences in the number
of deaths per treatments (Pearson χ2 = 5.389, p = 0.0676). However, mortality was more
likely in earlier instars (Pearson χ2 = 40.652, p < 0.0001): 64.5 % of the mortality occurred in
instar II, contrasted with much lower values in instars III (16.1 %), IV (9.7 %), V (6.5 %) and VI
(3.2 %).
33
CHAPTER 1
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
Discussion
Growth models for bridge spider development
Our feeding experiments revealed extraordinary developmental plasticity in the bridge
spider, L. sclopetarius, and a digress from various physiological rules. Our results are
contrary to Dyar’s (1890) and Przibram and Megušar’s (1912) widely accepted assumption
that growth ratios of successive instars are constant. Rather, we found that weight gain
over molts is exponential and thus follows a regular geometric progression. The growth
factor FG describes body weight increases between molts; the postulated growth factor of
2.0 (Przibram and Megušar 1912), was only found under low feeding conditions.
Depending on feeding conditions, FG can be larger (high food) or lower (very low food)
than 2.0. Hence the growth factor is influenced by feeding conditions and was 2.11 on
average in L. sclopetarius given our experimental conditions.
The relationship of weight and development time followed a power function, meaning
that weight gain in earlier instars is stronger than in later instars. The application of a
power function to describe weight gain over development time was previously suggested
by (Tammaru and Esperk 2007). We observed an overall decrease in growth ratios and an
increase in instar durations with successive instars. Hutchinson et al. (1997) reviewed the
literature on arthropod development to test their hypothesis that increase in size and
instar duration are optimized (Investment Principle). The Investment Principle explains
deviations from Dyar’s rule. Hutchinson et al. (1997) introduced the variable α that
describes the scaling of the rate of reserve accumulation with size. In arthropods, reserve
accumulation rises less than body size (α < 1). In case of high food availability (f in the
model of Hutchinson et al. (1997)), the Investment Principle predicts decreasing growth
ratios with consecutive instars. This prediction is confirmed experimentally by our results.
Several studies on other arthropods also found that body size increase decelerated with
increasing instars (Enders 1976, Klingenberg and Zimmermann 1992, Fantinou et al. 1996,
Higgins and Rankin 2001, Mayntz et al. 2003, Calvo and Molina 2008, Marczak and
Richardson 2008) while intermolt durations increased (Miyashita 1968, Mayntz et al. 2003,
Uhl et al. 2004). Thus, the application of Dyar’s rule for predictions of size and weight of
different instars during arthropod development is limited. We confirm the statement of
Klingenberg and Zimmermann (1992) on Dyar’s rule „as a base of comparison against
34
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
CHAPTER 1
which specific adaptive hypothesis can be tested, rather than to search for an adaptive
explanation for the rule itself“.
High plasticity in developmental parameters
Under varying feeding conditions L. sclopetarius showed high plasticity in all
developmental parameters: number of instars, growth factor (weight gain between molts),
aging factor (intermolt duration), and growth coefficient. Larinioides sclopetarius shows the
pattern of full plasticity in their postembryonic development (trajectory D in the
terminology of Higgins and Rankin (1996)).
Trap building animals such as spiders have only limited control over their foraging
success, which consequently may become unpredictable. Plasticity in life history traits
allows the animal to tolerate stochastic fluctuations in the number and quality of prey
items (Mayntz et al. 2003). Two other spider species, the orb-web spider Zygiella x-notata
(Mayntz et al. 2003) and the cursorial wolf spider Pardosa astrigera (Miyashita 1968), show a
similar degree of plasticity. Habitat and hunting strategies do not seem to drive these
similarities as Z. x-notata (and L. sclopetarius) occur in urban habitats (Mayntz et al. 2003),
while P. astrigera inhabits sunny open grasslands and hunts without a web (Miyashita
1968, Tanaka and Ito 1982, Tanaka 1993, Fujii 1998). Nevertheless, all three species share
the absence of strictly seasonal life cycles. In L. sclopetarius, all developmental stages are
present all over the year with a peak in summer (Schmitt and Nioduschewski 2007).
Zygiella x-notata has an annual life cycle with overwintering egg sacs but some females
survive through winter and built supplementary egg sacs in spring (Mayntz et al. 2003) .
Furthermore, the population dynamic changes with increasing prey abundance; they
reproduce earlier, and produce more and heavier eggs (Spiller 1992). In P. astrigera, there
are two peaks in population density of nymphs; one in spring and the other in fall
(Miyashita 1968). In contrast to the above examples, the golden orb-web spider Nephila
clavipes, which is canalized to change size in ecdysis (Higgins 1992, 1995) is strictly
seasonal (Higgins and Rankin 2001). These seasonal or non-seasonal life cycles may be
related to different prey availabilities and life history patterns. Plasticity is proposed to be
advantageous for non-seasonal species because it allows them to adapt to food
fluctuations throughout the year.
35
CHAPTER 1
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
Linking food availability to mortality
The high plasticity of L. sclopetarius appears to be associated with low mortality. Unlike
other animals (see Blanckenhorn 2005), L. sclopetarius did not show higher rates of
mortality when experiencing faster growth under laboratory conditions (i.e. without
predation) suggesting that there are no intrinsic physiological costs of fast growth.
However, mortality was very low in general across treatments (10.4% of all individuals) so
we cannot draw meaningful conclusions about the potential influence of growth speed
and mortality. In another spider species such as the golden orb-web spider N. clavipes
(Nephilidae), individuals that grow faster due to high prey availability suffer an increased
mortality risk (Higgins and Rankin 2001). Nephila clavipes tends to gorge food when prey is
very abundant (Higgins and Rankin 2001) and encounter problems during molts that cause
death. Under natural conditions, however, N. clavipes may not encounter sudden peaks in
prey densities so that there is no selection to adapt to such conditions. Similar to N.
clavipes, individuals of Tetragnatha versicolor died more frequently during molts under
high food conditions whereas total mortality was higher under restricted food conditions
due to unknown causes other than molting problems (Marczak and Richardson 2008).
Tetragnatha versicolor is sometimes found on riverbanks where, similar to the bridge
spider, it feeds on insects that emerge from the water. It may therefore encounter periods
of overabundance of prey (Marczak and Richardson 2008) when insects emerge in bursts.
However, since this is not their main niche (Aiken and Coyle 2000) it is possible that they
have not evolved a mechanism to counter overfeeding. Comparable to our results, T.
versicolor has variable growth rates and intermolt durations (Marczak and Richardson
2008). However, the total range of intermolt duration shows less variation (15-35 days) (see
Figure 3b in Marczak and Richardson 2008) than in L. sclopetarius (8-86 days). Bridge
spiders that live exclusively near water regularly experience an overabundance of prey due
to the seasonal and diurnal hatching synchrony of chironomid species (Chironomidae)
(spring, summer, and fall species) (Ziegler 2005). In particular, webs close to light sources
are often loaded with large numbers of freshly emerged insects. Webs with untouched
prey items are commonly observed (pers. observation).
Our results are based on continuous food regimes and it would be interesting to test
whether mortality would be different under varying prey conditions. Even though the
main prey of bridge spider underlies large seasonal fluctuations it is likely that these
36
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
CHAPTER 1
predators would easily cope since they can survive well in periods of starvation (as in our
treatment with very low prey).
What makes bridge spiders an invasive species?
Plasticity is advantageous in a variable and heterogenic environment (Caswell 1983,
Stearns 2000). Urban environments are probably not very variable but spatial heterogenic
for bridge spiders. Urban habitits act as heat islands with a reduced species diversity but an
increased species density (Shochat et al. 2006), favoring invasive colonization by plastic
organisms such as L. sclopetarius. Invasive species (plants and animals) are native or
nonindigenous species characterized by rapid proliferation allowing them to become
locally dominant and increase in abundance in a short time period (Richardson et al. 2000,
Kolar and Lodge 2001, Colautti and MacIsaac 2004). Shochat et al. (2006) recognized
developmental plasticity as a beneficial trait for urban species, in addition to resistance to
stress, disease and pollution. Plasticity will enable organisms to invade novel habitats
rapidly and effectively. The vast majority of invasive species studies deal with invasive
plants. And few studies propose general and consistent traits of invasive animals and of
those, most have focused on birds (Kolar and Lodge 2001). Larinioides sclopetarius shares
traits with invasive birds such as the production of several broods (or egg sacs, in the case
of spiders) per year. Other traits are similar to those of invasive plants. Invasive plants grow
in areas with high resource density and low predation (Blumenthal et al. 2009) and are
characterized by early flowering, high initial growth rate, and high reproductive output
(Garcia-Serrano et al. 2005). Similarly, L. sclopetarius experiences high prey densities when
living in proximity to streets and buildings where illumination attracts insects. In contrast
to many insects in cities that suffer high predation from birds (Shochat et al. 2006), L.
sclopetarius are nocturnal and hide in crevices during the day where birds cannot easily
access them. The short development in combination with the fact that egg development
does not require a cold period enables these spiders to multiply and their populations to
expand rapidly.
Phenotypic plasticity influences the invasiveness of plants if plasticity is related to
fitness (Richards et al. 2006) because it allows colonization of new habitats without
requiring environment-specific genetic adaptations (Sultan 2000). Although a comparison
between plants and spiders has limited utility, we propose a mechanism similar to that
37
CHAPTER 1
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
seen in plants that explains the extreme success of L. sclopetarius as an invasive species in
urban habitats.
Conclusion
Contrary to Dyar’s rule, growth ratios in Larinioides sclopetarius decrease with successive
instars. However, growth can be described by a geometric progression: either by an
exponential function for weight increase over instar or by a power function for weight
increase over development time. Bridge spider development shows full plasticity: all
developmental parameters, including growth factor (respectively growth coefficient), the
number of instars, and the aging factor, highly depend on food availability. High growth
rates due to overabundance of prey had no effect on mortality, suggesting that bridge
spiders experience no intrinsic physiological costs of fast growth. Accelerated growth,
earlier maturation, and thus rapid reproduction under high prey densities allow bridge
spiders to be an extremely successful invasive species in urban habitats. However, more
studies on a larger variety of taxa are desirable to establish an overall connection between
high developmental plasticity, invasiveness and urban habitats.
38
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
CHAPTER 1
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der Entomolgie. Spektrum Akademischer Verlag, Heidelberg.
44
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
CHAPTER 1
Appendix
Table 8 Feeding concept: the number of Drosophila melanogaster fed per week to spiders in
different treatments until maturation. Small values represent factors.
age since hatching [days]
feeding
level
15
59
60
119
120
179
180
239
240
299
300
359
≥360
ad libitum
high
low
3
1.7
5
1.6
8
1.9
15
1.4
21
very low
1
2.0
2
1.5
3
1.7
5
1.4
7
1.4
10
1.5
15
45
CHAPTER 1
46
DEVELOPMENTAL STRATEGIES IN AN INVASIVE SPIDER
Chapter 2
Evidence for Rensch’s rule in an orb-web spider
with moderate sexual size dimorphism
Abstract Body size, weight, and age at maturity are key life history parameters that
characterize lifecycles. They are determined by development and are highly relevant for an
individual’s fitness due to their effects on reproduction and survival. The sexes underlie
different selection pressures (fecundity selection vs. sexual selection), which usually results
in a sexual size dimorphism (SSD). Rensch’s rule, which states that male body size is more
variable than female body size, applies to many but not all taxa. In spiders, SSD is extreme
in cases of female gigantism and male dwarfism so that the assumptions of Rensch’s rule
are not met. However, it is unclear, whether the rejection of Rensch’s rule in spiders is a
general pattern or whether the better studied species with extreme reversed SSD are not
representative. Therefore, I selected a spider species with moderate SSD and a high
developmental plasticity to test sex specific variation in size and age at maturity. I
experimentally varied food supply during the development of the bridge spider Larinioides
sclopetarius and measured body size, body weight, and age at maturity for 267 male and
female spiders from 15 matrilines. My results support Rensch’s rule because only male
body size was affected by diet, while female body size was canalized. Females reacted to
decreasing food levels by prolonging developmental time and adding extra molts, while
males under poor diet were smaller than well-fed males despite adding extra molts and
increasing age at maturity. Interestingly, reaction norms of matrilines to different food
regimes differed suggesting a genotype × environment interaction. Unlike previously
assumed, my results show that Rensch’s rule is relevant for spiders, but perhaps only for
those species with no or reversed SSD.
47
CHAPTER 2
EVIDENCE FOR RENSCH’S RULE IN AN ORB-WEB SPIDER
Introduction
The body size of an organism is determined by the interaction of selective pressures that
can act in opposing or congruent directions: fecundity, sexual, and viability selection
(Blanckenhorn 2005). Selection on viability favors accelerated development and small
body sizes (Blanckenhorn 2000, 2005) because a prolonged growth period results in a
higher mortality risk due to predation, parasitism and starvation before the onset of
reproduction. Selection on fecundity acts only on females as the fitness advantage of more
and/or larger eggs and offspring favors enhanced growth since fecundity is often a direct
function of body size. In general, males are more often a target of sexual selection than
females (Roff 1992, Stearns 1992). Sexual selection and fecundity selection can oppose
selection on viability if costly traits are favored that increase mating and fertilization
success (equilibrium model of Arak 1988, Schluter et al. 1991, Fairbairn 1997, Blanckenhorn
2000, 2005).
Life history theory proposes a general and strong trade-off between size and age at
maturity because everything else being equal, more time is needed to grow larger. The
strengths of the various selection pressures and the balance between them naturally differ
between the sexes resulting in differences in size and age at maturity. A species is said to
exhibit sexual size dimorphism (SSD) if one sex is larger than the other (e.g. female spiders,
insects, fishes, amphibians, reptiles; male birds, mammals) (Darwin 1874, Arak 1988, Le
Boeuf and Reiter 1988, Shine 1988, Abouheif and Fairbairn 1997, Fairbairn 1997). Across
taxa, the degree of SSD increases with body size in case males are larger and it decreases
with body size in case of females are the larger sex, a pattern first described by Rensch
(Rensch 1959, Abouheif and Fairbairn 1997).
Fairbairn and Preziosi (1994) developed a quantitative explanation of Rensch’s rule by
regression of the logarithm of female body size within a group of taxa or populations over
the logarithm of male body size and showed that Rensch’s rule is supported if male body
size shows higher variability than female body size (Fairbairn and Preziosi 1994, Fairbairn
2005, Blanckenhorn et al. 2007).
Despite general support for Rensch’s rule in most taxa, several studies (Abouheif and
Fairbairn 1997, Fairbairn 1997, Foellmer and Moya-Laraño 2007) did not find allometry
patterns consistent with Rensch’s rule in spiders. Spiders are known for extreme SSD in
species with giant females and dwarf males (for review see Foellmer and Moya-Laraño
48
EVIDENCE FOR RENSCH’S RULE IN AN ORB-WEB SPIDER
CHAPTER 2
2007) and have often been used as model organisms in which to examine the proximate
causes for the evolution of SSD (Hormiga et al. 2000, Blanckenhorn et al. 2007, Foellmer
and Moya-Laraño 2007, Wilder and Rypstra 2008, Moya-Laraño et al. 2009). The allometry
patterns that are inconsistent with Rensch’s rule may result from large variation in female
size and an unusually weak correlation of male and female body size (Fairbairn 1997,
Foellmer and Moya-Laraño 2007, Kuntner and Coddington 2009). However, it is not clear
whether these are exceptions to the rule or not. Hence, Rensch’s rule may only be relevant
to spider taxa with weak or even male-biased SSD.
The bridge spider Larinioides sclopetarius shows only weak SSD; males and females
apparently have about the same body size. There are no confounding effects such as
sexual cannibalism, monogamous males, or maternal care that may alter selection
pressures on extreme SSD. Thus, any life history strategy of both sexes is likely to be
governed by the three major selection pressures (sexual, fecundity, and viability selection)
and growth patterns as well as variation in size, age, and weight at maturity.
The absence of an extreme female-biased SSD suggests that Rensch’s rule is applicable
for bridge spiders. Based on Rensch’s rule female body size is expected to be canalized due
to stabilizing selection (Fairbairn 2005). However, bridge spiders show tremendous
plasticity in all their developmental parameters (Chapter 1). This seems to be in contrast
with the expectation of a canalized female size at maturity.
The integration of high developmental plasticity with an expected rigidity in life history
traits and weak or no SSD makes bridge spiders an interesting model organism in which to
investigate patterns of life history evolution. We performed feeding experiments to
simulate three populations of bridge spiders with different food abundances to test for: (1)
the impact of developmental plasticity on three life history traits: size, weight, and age at
maturity; (2) sex related differences in these life history traits; and (3) sex specific responses
to variable feeding conditions. We predict that Rensch’s rule should apply to bridge
spiders and we expect to find stabilizing selection on female size. Further, we hypothesize
an increasing age at maturity in response to limited food. Stabilizing selection on body size
on the costs of age at maturity would reflect the balance between opposing selection for
fecundity and viability. We expect a different solution to the trade-off between size and
age at maturation for males. These differences between the sexes predict an interaction
49
CHAPTER 2
EVIDENCE FOR RENSCH’S RULE IN AN ORB-WEB SPIDER
between sex and feeding regime. Our results will contribute to the discussion on the
selective pressures influencing major life history traits in arthropods.
Methods
Study objects
The bridge spider Larinioides sclopetarius (Clerck, 1757) (Araneae: Araneidae) is a nocturnal
orb-web spider that is very abundant near water in urban habitats. Bridge spider colonies
comprise individuals of all developmental stages. We collected spiders in the HafenCity
Hamburg, Germany (53°33'N, 09°59'E) close to the River Elbe. Individuals were collected
from their webs on bridges and facades in 2006 from May to October and in April, 2007.
The spiders examined herein are the same individuals used in Chapter 1; details on
rearing conditions and feeding treatments are provided in that Chapter.
Rearing conditions
Field collected bridge spiders (parent generation) were kept individually in plastic cups
(females 400 ml, males 200 ml) and watered five times per week. Females were fed twice a
week with 3-5 Calliphora sp.; males were fed with 5-10 Drosophila melanogaster. After
maturation, females were transferred to Perspex frames (36 × 36 × 6 cm) where they built
their orb-webs and were mated. After mating, females were returned to plastic cups and
treated similar to pre-mating conditions. Plastic cups inhabited by mated females were
checked for the presence of egg sacs on five days per week. Egg sacs were weighed and
then kept in Perspex boxes (7 × 14.5 × 11.5 cm) under temperatures between 20 to 30 °C.
Egg sacs were watered five times per week until they hatched.
Feeding treatments
Ten days after hatching, fifteen full-siblings were randomly separated in three different
feeding treatments (high, low, and very low feeding conditions). Hatchlings for feeding
experiments were derived from 24 females with 15 maternal lines and are either the F1
generation or the F2 generation of the parent generation that was collected in the field
(for details see Chapter 1 appendix Table 9). Spiderlings with high feeding conditions
received Drosophila melanogaster ad libitum. In the low and very low feeding treatment,
50
EVIDENCE FOR RENSCH’S RULE IN AN ORB-WEB SPIDER
CHAPTER 2
food was limited. The first feeding was performed fifteen days after hatching: spiders with
low feeding level were fed three D. melanogaster, very low feeding level spiders received
one D. melanogaster per week. With increasing age of spiders until maturation, we
adjusted the number of fed D. melanogaster every 60 days by a factor of 1.5-2.
Spiderlings were fed twice a week, watered and checked five days per week for the
presence of exuviae. Spiders were weighed after each molt (post-molt weight) using an
electronic balance (METTLER TOLEDO XS105 DualRange) to an accuracy of 0.01mg.
Of 360 spiderlings in the experiment, 267 reached adulthood. We recorded the size,
weight, and age at maturity (i.e. development time) for each spider. Size at maturity was
measured after natural death of the spiders by measuring the tibia-patella length (TPL) of
the first pair of legs to the nearest 0.01 mm using a LEICA MZ 16 stereomicroscope and
LEICA IM500 imaging software (Version 4.0).
Statistical analysis
We used the REML (Restricted Maximum Likelihood) method for fitting mixed model
ANOVAs (Analysis of Variance) to estimate the effects of feeding treatment and sex on the
size, age, and weight at maturity. Feeding treatment and sex were fixed factors and family
was the random factor. All residuals were normally distributed, except for the age at
maturity (see Table 1). Further, the REML method was used to test the effects of
development time on size and weight at maturity within treatments and sexes.
Development time was the fixed factor; family was the random factor. An exclusion of the
family effects in all calculated models did not alter results. To test all differences among the
least square means in the model we used the Tukey’s HSD (Honestly Significant Difference)
test. The statistical analyses were performed using JMP® 7.0.2 (SAS Institute Inc.) for
Microsoft® Windows. For models that are fitted with the REML method, JMP® does not
calculate F-ratios or p-values for the random factor family.
Results
Size at maturity
Figure 1 and Table 1 show the relationship between size at maturity, feeding treatments,
and sexes. Size at maturity in bridge spiders was significantly influenced by feeding
treatment and sex. Bridge spiders under increased feeding conditions were larger than
51
CHAPTER 2
EVIDENCE FOR RENSCH’S RULE IN AN ORB-WEB SPIDER
those in other treatments, regardless of their sex. Feeding treatment influenced size at
maturity differently in the two sexes as reflected by the significant interaction between sex
and treatment. Males attained a larger maximum size with increasing feeding level and
reached a higher maximum tibia-patella length. Female size at maturity on average was
not influenced by the feeding treatments (Fig. 2).
The distribution of size classes (i.e. separation of size ranges in 11 classes) differed
between females and males (Fig. 3). Females that were reared in the high treatment
occupied the narrowest range of size classes (size at maturity ranged from 4.5 to 6.0 mm).
At low and very low feeding level the number of occupied classes increased; in the very
low feeding treatment the range of size classes was widest (size at maturity ranged from
3.5 to 6.25 mm). In male bridge spiders, the occupation of size classes was shifted towards
classes for larger sizes with increasing feeding level. The lowest classes were occupied by
individuals that were reared under limited feeding conditions (size at maturity ranged
from 4.25 to 6.5 mm); the highest classes were only occupied by spiders that had unlimited
food (size at maturity ranged from 5.0 to 7.0 mm).
Table 1 Results of ANOVA for the effects of feeding level (treatment) and sex on size, weight, and
age at maturity of spiderlings (N = 267).
size at maturity
variable
weight at maturity
age at maturity*
DF
F
p
F
p
F
p
treatment
2
10.22
<0.0001
61.71
<0.0001
1035.92
<0.0001
sex
1
50.00
<0.0001
293.08
<0.0001
59.38
<0.0001
sex ×
treatment
2
10.65
<0.0001
2.75
0.0656
11.41
<0.0001
* Residuals of age at maturity were not normally distributed. Re-analysis with a GLMM and Poisson distribution and a log link function
revealed the same results as the ANOVA. For simplicity we kept the ANOVA.
Weight at maturity
The relationship of weight at maturity with feeding treatments and sexes is shown in
Figure 1 with the statistical summary in Table 1. The weight at maturity depended
significantly on feeding treatment and sex. There was no significant interaction of sex and
treatment for the weight at maturity. Spiders that were reared under high feeding
52
EVIDENCE FOR RENSCH’S RULE IN AN ORB-WEB SPIDER
CHAPTER 2
conditions were about 25% heavier than spiders that grew under low or very low feeding
conditions. Regardless of feeding level, females were about 40% heavier than males.
Average values for the weight at maturity were 60 mg (SE ± 1.42) for females and 38 mg (±
size at maturity [TPL mm]
0.84) for males.
weight at maturity [mg]
6.5
a
b
b
a
6.0
6.0
5.5
5.5
5.0
5.0
4.5
4.5
4.0
4.0
80
a
b
b
b
80
a
70
70
60
60
50
50
40
40
30
30
20
20
b
350
350
age at maturity [days]
6.5
a
b
c
a
300
300
250
250
200
200
150
150
100
100
50
50
b
0
0
high low very low
feeding level
females males
sex
Fig. 1 Box plots for comparison of various life history traits of bridge spiders at different feeding
levels (left) and sexes (right). Box plots that are not connected by the same letter are significantly
different. Feeding level and sex influence all life history traits examined in this study. All values for
siblings within same treatment or sex were averaged.
Age at maturity
The effect of feeding treatment and sex on the age at maturity is shown in Figure 1 and
Table 1. Feeding treatment and sex significantly affected the age at maturity. Spiders that
were reared under high feeding conditions reached maturity at a younger age than spiders
under limited food. On average, spiders at high feeding level needed 71 days (± 2.33) until
maturation; under very low feeding conditions, the period from hatching to maturation
53
CHAPTER 2
EVIDENCE FOR RENSCH’S RULE IN AN ORB-WEB SPIDER
was extended by a factor of 3.7 (i.e. 269 ± 4.62 days). For females and males, the three
feeding treatments significantly influenced the age at maturity (Fig. 2). Males matured on
average 26 days earlier than females, however, under high feeding conditions, males and
females matured at the same age.
males
size at maturity [TPL mm]
females
weight at maturity [mg]
7.0
a
a
a
6.5
6.5
6.0
6.0
5.5
5.5
5.0
5.0
4.5
4.5
4.0
4.0
a
b
b
80
80
60
60
40
40
20
20
350
a
b
b
a
b
b
100
100
400
age at maturity [days]
7.0
400
a
b
c
350
300
300
250
250
200
200
150
150
100
100
50
50
0
a
b
c
0
high low very low
feeding level
high low very low
feeding level
Fig. 2 Box plots for comparison of various life history traits at different feeding levels in female (left)
and male (right) bridge spiders. Box plots that are not connected by the same letter are
significantly different. Feeding level influence all life history traits examined in this study similarly
for both sexes. Only the size at maturity of females is independent on food availability. All values
for siblings within same treatment and sex were averaged.
The impact of development time on size and weight at maturity
The size at maturity significantly depended on the development time, except for females
under high und males under low feeding conditions (Fig. 4, Table 2). For females on low
and females and males on very low feeding level, size was positively correlated with
development time. Males on high feeding level showed a negative correlation (Fig. 4).
54
EVIDENCE FOR RENSCH’S RULE IN AN ORB-WEB SPIDER
CHAPTER 2
Development time had a significant impact on the weight at maturity, except in the
case of female spiders at high feeding level (Fig 4, Table 2). For females and males under
low and very low feeding conditions, the weight at maturity increased with a prolonged
development time; males on high feeding level showed a decrease in weight at maturity
(Fig. 4).
males
feeding level
30
high
low
very low
25
20
number of individuals
number of individuals
females
15
10
5
0
4,5
4,75
5,5
25
20
15
10
5
0
4,75-5
5,75-6
6,25-6.56,56,75-77.0
4.254,25-4.5 4,54.75
5.05-5,25
5.255,25-5.55,5-5.75
6.06-6,25
6.25
6.75
3,75-44.0
4-4,25
4,25- 4.5
4,5- 4.75
4,75-5 5.0
5-5,255.25
5,25- 5.5
5,5- 5.75
5,75-6 6-6,25
3.53,5-3.75
4.25
6.0 6.25
3,75
30
5,75
4,5
4,75
size at maturity [TPL mm]
5,5
5,75
6,5
6,75
size at maturity [TPL mm]
Fig. 3 Distribution of size at maturity (tibia-patella length = TPL) in female (left) and male (right)
bridge spiders under varying feeding conditions (high, low, and very low). Females under very low
feeding conditions occupy all size classes observed; under high feeding conditions females occupy
a narrower range of size classes. Males under varying feeding conditions do not differ in the
number of size classes occupied. Small size classes are only occupied by poorly fed males; only
males under high feeding conditions attain the largest size classes.
Table 2 Results of ANOVA for the effect of age at maturity on size and weight at maturity, and the
effect of weight at maturity on size at maturity separated by feeding level (treatment) and sex of
spiderlings (N = 267).
females
feeding level DF
x
y
age at maturity
size at maturity
high
low
very low
age at maturity
weight at maturity
high
low
very low
males
F
p
F
p
1
1
1
0.81
14.38
35.83
0.3752
0.0005
<0.0001
10.43
0.21
15.31
0.0028
0.6522
0.0008
1
1
1
0.46
61.20
43.04
0.4995
<0.0001
<0.0001
11.68
39.64
20.49
0.0020
<0.0001
<0.0001
55
CHAPTER 2
EVIDENCE FOR RENSCH’S RULE IN AN ORB-WEB SPIDER
size at maturity [TPL mm]
7.0
6.0
5.0
4.0
high
low
very low
3.0
size at maturity [TPL mm]
A
females
8.0
7.0
6.0
5.0
4.0
3.0
2.0
2.0
0
50
100
150
200
250
300
350
0
400
50
100
100.0
80.0
60.0
high
low
very low
40.0
20.0
weight at maturity [mg]
B
120.0
weight at maturity [mg]
males
8.0
150
200
250
300
350
300
350
males
120.0
100.0
80.0
60.0
40.0
20.0
0.0
0.0
0
50
100
150
200
250
300
350
400
0
development time [days]
50
100
150
200
250
development time [days]
Fig. 4 Regression plots for the impact of development time on size (A) and weight (B) at maturity in
female (left) and male (right) bridge spiders. Filled squares and solid line represent high feeding
level, open circles and dashed line low feeding level, filled triangles and dotted line very low
feeding level. Development time influences weight and size at maturity depending on feeding
treatment and sex. All values for siblings within the same treatment and sex were averaged.
Family × treatment interactions
In each family there were three possible strategies in reaction to feeding treatment: first,
the values for the life history traits size, weight, or age at maturity decreased with
decreasing feeding level (solid line); second, the life history trait increased with decreasing
feeding level (dashed line); and third, decrease and increase in the life history trait
alternated between feeding levels (dotted line) (Fig. 5).
All three strategies were represented in the size at maturity in females. In four families,
females increased their size with decreasing food, five families exhibited the inverse trend,
and the other families did both. Males from five families decreased their size with
decreasing food; one family showed an increase in size with decreasing food. None of the
families showed an increase in weight with reduced feeding condition: either the weight
decreased or there was no clear trend for increasing feeding level. This was true for females
and males.
In all families, the effect of feeding condition on age at maturity was similar: they show
an increase in age at maturity with decreasing feeding level, independent of sex. The
56
EVIDENCE FOR RENSCH’S RULE IN AN ORB-WEB SPIDER
CHAPTER 2
number of molts generally increased under limited food in both sexes. Some families
showed an alternating response to different feeding conditions.
weight at maturity [mg]i
size at maturity [TPL mm]
females
males
6.5
6.5
A
6.0
6.0
5.5
5.5
5.0
5.0
4.5
4.5
4.0
4.0
3.5
3.5
100
100
B
90
80
70
70
60
60
50
50
40
40
30
30
20
20
10
10
400
age at maturity [days]i
90
80
400
C
350
350
300
300
250
250
200
200
150
150
100
100
50
50
0
0
number of molts
10
10
D
9
9
8
8
7
7
6
6
5
5
4
4
high
low
very low
high
low
very low
feeding level
Fig. 5 Genotype by environment interactions for size at maturity (A), weight at maturity (B), age at
maturity (C), and the number of molts (D). There are three possible reaction norms for individuals
within families (i.e. genotypes) in response to different feeding treatments (i.e. environment): first,
the life history trait (size, weight, or age at maturity) decreases with decreasing feeding level (solid
line); second, the life history trait increases with decreasing feeding level (dashed line); and third,
the life history trait decreases and increases between feeding levels (dotted line). Only genotypes
that were represented by at least one individual within each treatment were considered.
57
CHAPTER 2
EVIDENCE FOR RENSCH’S RULE IN AN ORB-WEB SPIDER
Discussion
Our study verified a considerable impact of feeding treatments on major life history traits
such as size, weight, and age at maturity of Larinioides sclopetarius. Size, weight, and age at
maturity differed between male and female bridge spiders but differences in food
availability had similar effects on life history traits for males and females, except for the size
at maturity in female bridge spiders, which was unaffected by juvenile food availability. In
accordance with our predictions we found evidence for stabilizing selection on female size
at maturity. Trade-offs between development time (age at maturity) and size as well as
weight at maturity were apparent in the food-restricted treatments and females showed a
stronger relation (steeper slopes, Fig. 4) between size and weight at maturity over
development time than males. We showed that the parentage of L. sclopetarius individuals
influenced the reaction norm to alternating prey abundances.
Impact of food availability on life history traits
Bridge spiders that were raised under unlimited food availability grew larger and heavier
and reached maturity at a younger age than individuals under limited food treatments.
Similar results were reported for Zygiella x-notata (Araneidae) (Mayntz et al. 2003) and
Pholcus phalangioides (Pholcidae) (Uhl et al. 2004). However, this pattern is not generally
applicable to spiders: in Lycosa tarantula (Lycosidae), spiders that were reared with limited
food were younger at maturity than individuals at high feeding level (FernándezMontraveta and Moya-Laraño 2007). We suggest that there are two different strategies in
response to limited prey abundances, either by optimizing the size at the expense of
development time (L. sclopetarius, Z. x-notata, P. phalangioides) or by optimizing
development time at the costs of size (L. tarantula). Thus, there might be differences in the
relative selection strength for body size and timing of maturation that may be related to
seasonality. If seasonality influences developmental strategies, we would expect for
spiders with a short reproductive seasonal timeframe that selection constraints
development time on the expense of size. In L. sclopetarius, seasonality and timing of
reproduction might be less important for reproductive success than size at maturity.
58
EVIDENCE FOR RENSCH’S RULE IN AN ORB-WEB SPIDER
CHAPTER 2
Sex specific differences in bridge spiders
Weight: Females of L. sclopetarius are heavier than males although in Chapter 1 we showed
that the growth rate (i.e. the weight gain over instars) shows no significant difference
between males and females. The combination of a similar growth rate for the sexes with a
longer development time for females inevitably results in females becoming the heavier
sex at maturity.
Size: Male L. sclopetarius have a larger size (leg length) than females despite the shorter
development time. Males are lighter at maturity, and as demonstrated in Chapter 1 pass
through fewer instars. However, the male-biased sexual size dimorphism (SSD) in bridge
spiders is moderate; the difference between sexes in leg length is about 10%.
Males invest more in body size and shorten developmental time through minimising
the number of instars required at maturation. Females invest in weight gain and in size but
grow more slowly. These differences follow the general pattern of females’ maximising
fecundity and males maximising body size. Spider species differ in the components and
strength of sexual selection but large male body size is favoured under contest
competition and under female choice. Male-male and female-male interactions were not
the focus of this paper, however, male-male competition in bridge spiders is repeatedly
observed in the field and during mating in the laboratory. It is often observed that several
males court a single female (pers. observation). Thus, sexual selection, either by contest
competition or female choice, might be a mechanism to increase male body size.
Besides sexual selection, male size is believed to be also a target of natural selection
(Blanckenhorn 2000, 2005, Huber 2005). The effect of natural selection on the leg length of
male spiders was previously demonstrated for Argyoneta aquatica (Cybaeidae). An
increased leg length was proposed to increase the mobility of males under water (Schütz
and Taborsky 2003). However, underwater locomotion is considerably different from
terrestrial locomotion: on land, usually the smaller males are more mobile (Foelix 1996).
That natural selection resulted in elongated leg length in male L. sclopetarius remains
speculative at the moment.
Development time
In L. sclopetarius, males were protandrous with a shorter development time than females.
Protandry is frequently observed in spiders (LeGrand and Morse 2000, Maklakov et al. 2004,
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EVIDENCE FOR RENSCH’S RULE IN AN ORB-WEB SPIDER
Uhl et al. 2004). In seasonal species, protandry was hypothesized to be advantageous if: (1)
females are more abundant early in the season (Andersson 1994), (2) mating occurs
immediately after female molting (Robinson and Robinson 1980, Miyashita and Hayashi
1996, Foellmer and Fairbairn 2003), (3) mate-guarding takes place (Fromhage and
Schneider 2005, Kuntner et al. 2009), and (4) first male priority occurs (Drengsgaard and
Toft 1999). However, bridge spiders are non-seasonal (Chapter 1), and selective pressures
for protandry are less obvious. In bridge spiders, receptive females are present throughout
the year, due to overlapping generations. Thus, protandry likewise has no or little
relevance for competition for females. We assume a connection between the shorter
development time and the reduced weight at maturity of males (40% of female weight).
Males are suggested to be lighter (and thus faster in development) because they have to
allocate fewer resources for sperm production than females do in ova production (Darwin
1874, Andersson 1994).
Blanckenhorn et al. (2007) hypothesized, that differences in growth rate, rather than
development time, are generally responsible for SSD. Our results on bridge spiders confirm
the hypothesis by Blanckenhorn et al. (2007). Further, Blanckenhorn et al. (2007) showed
that SSD in spiders was more related to differences in development time compared to
other arthropods. However, in L. sclopetarius, the size differences between males and
females are independent of differences in development time. On the contrary, although
males develop faster, they are larger, in other words the shorter development time is
overcompensated by a higher growth rate. The species of the Araneae in the study of
Blanckenhorn et al. (2007) all had a female-biased SSD. However, in some arthropod
species with male-biased SSD, males showed a tendency to grow faster than females
(Blanckenhorn et al. 2007). This is analog to our results for bridge spiders and could be a
more general trend for arthropods with male-biased SSD.
Sex specific differences in response to food availability
Female size at maturity is independent of food availability but the range of sizes varied
with different prey abundances. In the high feeding treatment, more females reached the
average (presumably “optimal”) size than under low or very low feeding conditions; the
range variation in size at maturity is lower for females with unlimited food. By increasing
the development time, females under limited feeding conditions potentially reach the
60
EVIDENCE FOR RENSCH’S RULE IN AN ORB-WEB SPIDER
CHAPTER 2
same size on average as females with unlimited food. These results show that high
developmental plasticity does not necessarily force life history traits to be variable.
In contrast to females, male size at maturity did depend on the feeding treatment: a rich
diet increases male leg length. Based on the assumption that body size in males and
females is under different selective pressures (Blanckenhorn 2000, 2005), we suggest for L.
sclopetarius that natural selection acts to stabilize female body size, while sexual selection
acts directional to increase male body size. The comparatively higher variance of male size
over female size in bridge spiders is consistent with Rensch’s rule (Rensch 1950, Fairbairn
2005). This is surprising, because Rensch’s rule was regularly found to not apply to spiders
(Foellmer and Moya-Laraño 2007), except for Lycosa tarantula, which had female-biased
SSD consistent with the rule (Fernández-Montraveta and Moya-Laraño 2007). Our results
present the first evidence for Rensch’s rule in a spider species with male-biased SSD.
Trade offs and genotype × environment interactions
The well-established life history trade-offs between age and size at maturity, and between
age and weight at maturity do not apply for female and male L. sclopetarius under
unlimited feeding conditions. A decrease in age at maturity is predicted to result in
decreasing size and weight at maturity (Roff and Fairbairn 2007). Under unlimited food,
however, for female bridge spiders there is no relationship between development time
and either size or weight at maturity; in males, size and weight at maturity decrease with
increasing age at maturity (Fig. 4).
The discrepancy between these expectations and our results may be due to two
reasons: (1) a direct genetic impact on life history traits, and (2) genotype × environment
interactions.
This study did not investigate genetic effects: if we separate the data into genetic
lineages, the number of replicates is too low for robust statistical analyses on genetic
effects. However, a preliminary statistical analysis that included only genetic lineages that
were represented by at least three females and three males in each feeding treatment
suggested a potential relationship between female, but not male, parentage and size or
weight.
Genotype × environment interactions (GEI) describe variable responses to alternating
environmental conditions by different genotypes (Falconer 1952, Via and Lande 1985).
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There are two opposite patterns of reaction based on two proposed genotypes in L.
sclopetarius (Fig. 5): (1) decrease of size and weight under limited feeding conditions
(genotype I) and (2) increase of size and weight under limited feeding conditions
(genotype II). Relative to individuals with genotype I, individuals with genotype II increase
their number of molts substantially in favor of larger sizes and greater weights if exposed
to decreased prey abundances.
The decrease in male size and weight with increasing age that was observed under
unlimited feeding conditions might also be explained by GEI. Genotype I individuals may
be optimized for fast development under high prey abundances and reach larger sizes.
Males with genotype II will perform better under limited food conditions but worse with
rich diet and thus be smaller even after longer development time. In spiders with genotype
I, faster growth and thus earlier reproduction, can have a negative genetic correlation with
longevity (Blanckenhorn 2000). Natural environments of bridge spiders are very
heterogeneous; foraging sites can differ extremely in their quality (Heiling 1999, Schmitt
2004, Schmitt and Nioduschewski 2007a, Schmitt and Nioduschewski 2007b). This may
select for some genotypes adapted to lower prey abundances thus avoiding intraspecific
competition for high resource localities.
Conclusion
Our feeding experiment distinguished influences of prey abundance on major life history
traits, including size, weight, and age at maturity in the bridge spider L. sclopetarius. High
prey abundance resulted in larger and heavier spiders that reached maturity at a younger
age, than spiders under limited food availability. Males and females show similar responses
in their life history traits to variable prey availabilities, except in the case of size, where
female spiders are canalized. We argue that the size at maturity of female spiders is under
stabilizing selection and showed on average no response to different feeding conditions.
In contrast, males showed more variability in their size, a pattern consistent with Rensch’s
rule. The comparison of males and females in our study exposed a male-biased sexual size
dimorphism in bridge spiders, although males are the lighter sex with shorter
development time. Thus, this makes bridge spiders the first documented case of malebiased SSD in combination with Rensch’s rule in spiders. Future analysis of whether
Rensch’s rule is applicable to spiders should therefore not focus exclusively on species with
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EVIDENCE FOR RENSCH’S RULE IN AN ORB-WEB SPIDER
CHAPTER 2
extreme cases of female-biased SSD but should also include spiders with weak or malebiased SSD.
In addition to sex-related responses to variable environments, we also found genotype
× environment interactions (GEI) in L. sclopetarius. Based on GEI, we propose the presence
of two different life history strategies that are optimized for different environments.
Genotypes may differ in their resource allocation: the genotype that will be outcompeted
under rich diet could be beneficial under poor diet and vice versa. The combination of high
phenotypic plasticity with possible variations in genotypes, may allow bridge spiders to be
an extremely successful species in heterogeneous environments. However, the adaptive
significance of GEI remains to be justified by future studies. Further, the mechanism that
underlies GEI needs to be resolved. The integration of experimental life history research
with molecular biology to explain different responses to variable environments will
potentially reveal new insights in the evolution of life histories.
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Chapter 3
Dietary restriction increases lifetime fecundity
and extends lifespan in a spider
Abstract The reproductive success (measured as lifetime fecundity) of an organism is
determined by complex interactions of (i) the life history traits size, weight, and age at
maturity, (ii) lifespan, and (iii) the respective trade-offs, as a benefit for one trait might
entail a cost for another. Depending on environmental factors such as food availability,
population density, and temperature, the reaction norm of life history traits will evolve to
increase lifetime fecundity. This may result in the evolution of prolonged lifespans under
poor feeding conditions. However, the effects of environmental factors likely differ in
different life stages, such as developmental and reproductive periods. Thus, to draw a
complete picture about the interactions between life history traits and environmental
factors, it is essential to examine all periods of an individual’s life. Here we investigate the
impact of diet (before and after maturation) on lifetime fecundity in a highly
developmentally plastic organism – the bridge spider, Larinioides sclopetarius. This species
is known to respond to variable prey abundances during development by flexibly adapting
growth patterns and life history traits at maturity. By changing food regimes after
maturation, we demonstrate the absence of interactions between food availability during
development and adult life stages. Females that experience low food and a long
development are able to catch up to higher number of offspring during their reproductive
stage if conditions improve. We show that a rich diet during development and
reproduction increases lifetime fecundity and shortens lifespan while egg weight is not
affected. This suggests that diet increases offspring quantity but has no effect on offspring
quality. Offspring quantity and quality are traded-off as larger clutches contain lighter
eggs. Furthermore, we found that egg weight is influenced by whether the egg is fertilized
or not. In contrast to well-fed spiders, spiders that experienced a poor diet partly
compensate for their delayed development by slowing down senescence and yet they still
exhibit a lower lifetime fecundity.
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Introduction
Age and size at maturity, number and size of offspring, and the reproductive lifespan and
aging are the major life history traits (Stearns 1992). These traits are interrelated to each
other and relations between different traits are complex. For example body size and
fecundity (i.e. number of offspring) are often positively related (Wickman and Karlsson
1989, Honek 1993, Marshall and Gittleman 1994, Head 1995, Foellmer and Moya-Laraño
2007); whereas reproductive effort has been shown to decrease lifespan (Austad 1989).
Individuals regularly encounter trade-offs among life history traits, because resources
that are invested to the benefit of one trait cannot be allocated to another. For example, a
well documented trade-off exists between the number (quantity) and size (quality) of
offspring. Another fundamental trade-off involves size and age at maturity; individuals that
mature earlier are smaller (Roff 1980, Roff 1992).
In addition to these complex relationships between different life history traits, there are
even more complex interactions with environmental factors such as temperature, density
and food availability. The impact of food availability on the life history of organisms is well
studied and can influence size, weight, and age at maturity, number and size of offspring
as well as the lifespan itself. The size and weight at maturity of animals may increase with
greater food availability and well-fed individuals often mature at a younger age (Roff 1992,
Blanckenhorn 1998, Mayntz et al. 2003, Uhl et al. 2004, Marczak and Richardson 2008).
Increased food may directly translate into increased numbers of offspring although this is
not generally true (Wise 1979, Sota 1985, Parker and Begon 1986, Pékar 2000, Agarwala et
al. 2008). Conversely, limited feeding conditions tend to increase the lifespan of animals
(Austad 1989, Masoro 2005). The interrelations between life history traits can cause a
consecutive reaction: if environmental factors impact one particular trait, other traits are
subsequently, but indirectly affected.
Individuals may react differently to environmental factors, depending on their life stage
(i.e. growth or reproduction period). Many predators change their range of prey
throughout their lives. Larger individuals can handle larger prey items than smaller
conspecifics (Enders 1976, Hutchinson et al. 1997). In some extreme cases, the dietary
spectrum shifts completely (many holometabolous insects after maturation, Labandeira
1997), or feeding stops after maturation (e.g. mayflies Sternfeld 1907, adult male wasp
spiders Foelix 1996). Thus, because of the exploitation of different food resources, the
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DIETARY RESTRICTION INCREASES LIFETIME FECUNDITY AND EXTENDS LIFESPAN
CHAPTER 3
periods of growth and reproduction will be affected differently by prey fluctuations.
However, the differential effects of diet on life history traits during different life stages are
poorly known.
Orb-web spiders are suitable models to address diet effects on life history traits over life,
as they are sit-and-wait predators and thus are directly affected by variation in prey
densities (Anderson 1970, Mayntz et al. 2003). Furthermore, some species, such as the
bridge spider Larinioides sclopetarius, show extraordinary levels of developmental plasticity
in response to variable diets (Chapter 1, 2). In this species only the body size of females was
canalized, all other life history traits (growth pattern, age and weight at maturity) were
highly variable in response to diet (Chapter 2). But how this plasticity and different
responses to variation in prey abundance affect lifetime reproductive success and lifespan
is not known.
Here we examine the lifetime fecundity and lifespan of female bridge spiders that were
reared under laboratory conditions and observed until death. Because adult males do not
construct orb-webs and controlled feeding is difficult, we focus on females. We varied the
food supply before (i.e. development) and after maturation (i.e. reproduction) to
investigate the impact of food availability on reproductive performance and lifespan. For
females under high feeding conditions after maturation we predict a higher number of
offspring in a shorter reproductive period. Because we previously found no impact of
feeding regime on female body size (Chapter 2), we expect female fecundity to be
independent on juvenile feeding level. However, based on the observation that
development is prolonged under poor diet (Chapter 1), we predict a shorter reproductive
period that should result in a decreased fecundity. These contradictive predictions may
reflect a trade-off between size and age at maturity, which effects lifetime fecundity under
variable environmental conditions.
Methods
Study objects
The bridge spider Larinioides sclopetarius (Clerck, 1757) (Araneae: Araneidae) is a
synthropic orb-web spider, which is very abundant near water. The parent generation of
the laboratory stock of bridge spiders was collected from bridges and facades in the
HafenCity Hamburg, Germany (53°33'N, 09°59'E). Details on origin and maternal lines are
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presented in Chapter 1. We observed the life of spiders from birth until death under
controlled laboratory conditions from August 2006 to November 2008.
Feeding experiment
We followed 119 females throughout their lives. The spiders were reared under three
different juvenile feeding conditions (high, low, and very low). For juvenile treatments, 15
spiderlings per egg sac of 24 females were randomly separated in the three feeding
treatments 10 days after hatching. They were fed with different amounts of Drosophila
melanogaster (high – ad libitum; low, very low – restricted) until sexual maturation. The
juvenile feeding treatments are described in detail in Chapter 1 and 2. Immediately after
maturation, each juvenile feeding treatment was randomly divided into two separate adult
feeding treatments (high and low feeding level). Adult female spiders were fed with one
blowfly (Calliphora sp.) daily (high feeding level) or weekly (low feeding level). The spiders
were kept individually in plastic cups (400 ml) and watered five days a week.
Table 1 Experimental design for feeding treatments throughout life in bridge spiders.
feeding treatments
maturation
juvenile
adult
high
high
low
very low
low
Mating
Females were transferred to plastic frames (36 × 36 × 6 cm) where they built their orb webs
and were mated seven days after maturation. Males were introduced into the web and
removed after copulation was observed or after 3 days if copulation did not occur
immediately. Fertilization was successful in most cases although 15 spiders laid unfertilized
egg sacs. Twelve females died before they produced an egg sac. All female spiders were
continuously fed according to their feeding treatments until they died. After mating
females were transferred to upturned plastic cups (400 ml), which were visually inspected
for the presence of egg sacs five days per week.
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DIETARY RESTRICTION INCREASES LIFETIME FECUNDITY AND EXTENDS LIFESPAN
CHAPTER 3
Incubation
Newly laid egg sacs were removed from the plastic cups, the dates were noted, and the
egg sacs were weighed after the silk was removed. After weighing, the egg sacs were
transferred to individual boxes and incubated under different temperatures (in climate
chambers at 8, 20, 25, 30, 35°C or in the laboratory under room temperature of 20-25°C).
Boxes with egg sacs were watered and inspected for the presence of hatched spiderlings
five days per week.
The first day that spiderlings were present was noted as the hatching date. Most of the
time, all spiderlings hatched on the same day, however on occasion, we found differences
of up to three days in the hatching time of spiderlings from the same egg sac. To ensure
that all spiderlings hatched from an egg sac and because handling of second instar
spiderlings was easier, we waited approximately ten days and then counted all spiderlings
and the remainder (unhatched/unfertilized) eggs.
Data recording
We recorded weight, and age at maturity for each individual (see Chapter 2 for details) and
adult size by measuring the tibia-patella length (referred to as ‘leg length’) of the first pair
of legs after the females died. This sclerotized body part does not change in size after the
final molt.
After the females matured, we recorded: reproduction time (i.e. the time span from
maturation to death), lifetime fecundity (total clutch size), number of egg sacs, fertilization
success (i.e. the ratio of fertilized vs. unfertilized eggs within an egg sac), egg weight (i.e.
the ratio between the weight of the egg sac and the total number (fertilized and
unfertilized) of eggs), and the time interval between clutches including the time from
copulation to first egg deposition. Unfertilized eggs were identified beyond doubt by
comparison with egg sacs that were built by unmated females. Development time until
maturation plus the reproduction time equals the total lifetime.
Statistical analysis
We used the REML (Restricted Maximum Likelihood) method for fitting mixed model
ANOVAs (Analysis of Variance) to estimate the effects of (1) juvenile and adult feeding
conditions and (2) size, weight, and age at maturity on female reproduction time, female
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lifespan, lifetime fecundity, number of egg sacs a female produces, mean weight of eggs
from egg sacs with 100% fertilization success, and the mean interval between subsequent
depositions of egg sacs. Feeding treatments and the life history traits size, weight, and age
at maturity were fixed factors; family IDs were random factors.
We tested the residuals for normal distribution by applying the Shapiro-Wilk test. In
cases where the distribution of residuals deviated from normal, we log transformed the
data and repeated the test. In only a few cases residuals were non-normally distributed,
but after visual inspection we picked the data type (original or log transformed) that was
closest to a normal distribution, because it was previously shown that ANOVAs are robust
to minor deviations from normal distributions at large sample sizes (Sokal and Rohlf 1995).
Table 2 shows whether the data were normally distributed and which type of data was
used.
For individual pairwise comparisons of least square means in the model we used
Student’s t-test. To test all differences among the least square means we used the Tukey’s
HSD test (Honestly Significant Difference). The statistical analyses were performed using
JMP® 7.0.2 (SAS Institute Inc.) for Microsoft® Windows. For models which are fitted with the
REML method, JMP® does not calculate F-ratios or p-values for the random factor family.
Results
We detected no significant interactions between juvenile and adult feeding treatment on
any of the reproductive parameters or overall lifespan (Table 2) and thus considered both
treatments separately.
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CHAPTER 3
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Lifetime fecundity
Lifetime fecundity (i.e. the total number of eggs laid during life) depends on the number of
clutches and on the numbers of eggs within each of the clutches and varied between 8
and 1,787 eggs. On average females produced 6 (± SE 0.34, range 1-15) egg sacs in their
lifetime independent of feeding level. Hence the variation in lifetime fecundity is mainly
due to variation in the number of eggs per clutch and not the number of clutches. The
number of clutches was influenced only by the age at maturity such that females that
developed more slowly produced fewer egg sacs (Fig. 1, Table 2).
Clutch size is directly and positively affected by the juvenile and the adult feeding
treatment and is positively related to size and weight at maturity (although the correlation
between weight and lifetime fecundity is not significant) (Fig. 2, Table 2). Interestingly,
slow growing females had lifetime fecundity costs even though their size at maturity was
not different from fast growing females (Chapter 2), suggesting a reproductive cost of
decelerated development (Fig. 3, Table 2).
number of egg sacs
16
14
12
10
8
6
4
2
0
0
p = 0.0475
100
200
300
age at maturity [days]
400
N = 119
Fig. 1 Relationship of the total number of egg sacs and the age at maturity in bridge spiders. An
increased age at maturity increases the number of egg sacs a female produces during life.
Intervals between clutches
The time between consecutive egg sacs varied between 2 and 132 days and was only
affected by adult feeding treatment (Table 2). Females in the high feeding treatment had a
significantly shorter mean interval between egg sac deposition than females under limited
feeding conditions (Fig. 4, Table 2), suggesting that egg production is a direct function of
the immediate nutrition.
76
DIETARY RESTRICTION INCREASES LIFETIME FECUNDITY AND EXTENDS LIFESPAN
CHAPTER 3
juvenile
lifetime fecundity
2000
adult
a
a
ab
b
high
low
very low
b
1500
1000
500
0
high
low
feeding level
N = 119
Fig. 2 Box plots for comparison of the effects of different juvenile (left) and adult (right) feeding
conditions on lifetime fecundity. Box plots that are not connected by the same letter are
significantly different. Food availability during development and reproduction influences lifetime
fecundity of female bridge spiders. Limited food results in lower fecundity.
4
3
3
2
2
1
4
(total clutch size)
4
1
N = 117
0
3.5
4
4.5
5
5.5
size at maturity [TPL mm]
6
2
1
N = 119
0
6.5
3
N = 119
0
20
p = 0.0035
40
60
80
100
weight at maturity [mg]
p = 0.0538
0
100
200
300
age at maturity [days]
400
p = 0.0018
Fig. 3 Relationship of the logarithm of lifetime fecundity and life history parameters size (TPL =
tibia-patella length), weight, and age at maturity. Increased size and decreased age at maturity of
bridge spiders increase lifetime fecundity significantly. An increased weight at maturity has the
tendency to increase lifetime fecundity.
mean interval between
egg sacs [days]
60
juvenile
adult
a
a
a
high
low
very low
a
b
50
40
30
20
10
0
high
feeding level
low
N = 105
Fig. 4 Box plots for comparison of the mean interval between egg sacs of bridge spiders at
different feeding levels during juvenile and adult life. Box plots that are not connected by the same
letter are significantly different. Increased feeding condition after maturation decreases the mean
interval between successive clutches. The feeding condition during growth has no influence on the
interval between egg sacs.
77
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DIETARY RESTRICTION INCREASES LIFETIME FECUNDITY AND EXTENDS LIFESPAN
Egg weight and embryonic development
The mean egg weight of a clutch (clutch weight/clutch size) significantly depended on the
fertilization success (ANOVA, F1,638=606.52, p<0.0001). Fertilized eggs had about twice the
weight of unfertilized eggs (Fig. 5). Mean weight of fertilized eggs (only egg sacs with
100% fertilization success considered) was significantly and negatively correlated with
clutch size (ANOVA, F1,127=6.60, p<0.0114) (Fig. 6).
The egg weight produced by each female per egg sac was independent of the feeding
treatment (juvenile and adult; Fig. 5, Table 2), independent of the size, weight, and age at
maturity of the female (Table 2), and did not vary with the order number of egg sacs
(Wilcoxon two sample test, χ28,127=4.15, p=0.8433).
Depending on the temperature, spiderlings hatched after an embryonic development
time of 7.6 to 18.6 days. Embryonic development until hatching was significantly faster for
egg sacs that were kept under higher temperatures (Mann-Whitney test, χ24,355=255.77,
p<0.0001, Table 3). Temperatures of 8 and 35 °C were lethal for embryonic development.
Under constant temperature (25 °C) the embryonic development time was not influenced
by the egg weight (of egg sacs with 100% fertilized eggs) (ANOVA, F1,53=1.22, p=0.2737).
mean egg weight [mg]
3.0
2.5
2.0
1.5
1.0
0.5
0.0
0%
p < 0.0001
20%
40%
60%
80%
egg sac fertilization success
100%
N = 638
Fig. 5 The impact of egg sac fertilization success on mean egg weight. The mean egg weight within
an egg sac increases depending on the number of fertilized eggs.
78
DIETARY RESTRICTION INCREASES LIFETIME FECUNDITY AND EXTENDS LIFESPAN
0.4
0.3
0.2
0.1
0.0
-0.1
-0.2
-0.3
0
50
p = 0.0114
100
150
clutch size
200
of 100% fertilized egg sacs
mean egg weight [mg]
(100% fertilized egg sacs)
juvenile
2.0
0.5
log mean egg weight
CHAPTER 3
250
adult
a
a
a
high
low
very low
a
a
1.8
1.6
1.4
1.2
1.0
0.8
0.6
high
feeding level
N = 127
low
N = 54
Fig. 6 The relationship of clutch size and log mean egg weight (left) and the effect of different
feeding levels (juvenile and adult) on mean egg weight (right). In case a female produces more
than one 100% fertilized egg sac, the mean egg weights were averaged for box plots. Box plots
that are not connected by the same letter are significantly different. In egg sacs that have 100%
fertilized eggs, (1) the mean egg weight within an egg sac decreases with increasing clutch size; (2)
the mean egg weight is not under the influence of food availability during life.
Table 3 Influence of egg sac incubation temperature on embryonic development time in bridge
spiders (N = 355).
incubation temperature [°C]
8
20
25
30
35
mean embryonic
development time [days]
-
18.6
±0.17
11.1
±0.12
7.6
±0.18
-
Reproduction time and lifetime
The duration of reproduction time (i.e. the time from maturation to death) depended
significantly on the feeding conditions during juvenile growth and after maturation (Table
2). Juvenile and adult feeding treatments had a reciprocal effect on reproduction time:
females that were reared under high feeding conditions had a longer reproduction time
than females under limited food during development, however, after maturation,
increased food availability resulted in shorter reproduction times (Table 2, Fig. 7).
Reproduction time is significantly and negatively influenced by the age at maturity but
independent of the size and weight at maturity. Females that were older at maturity had a
significantly shorter reproduction time (Table 2, Fig. 7).
The total lifetime of female bridge spiders highly depended on the feeding conditions:
spiders that had unlimited feeding conditions during development and reproduction (high
lifetime feeding conditions) reached a mean age of 240 days; spiders under limited food
79
CHAPTER 3
DIETARY RESTRICTION INCREASES LIFETIME FECUNDITY AND EXTENDS LIFESPAN
during development and reproduction died on average 420 days after hatching (Table 2,
Fig. 7).
maturation
-400
-300
-200
-100
development time [days]
0
feeding level
juvenile adult
100
200
300
400
hhhigh
HLhigh
LHlow
LLlow
very low
VLH
vllvery low
hh
HL
LH
LL
VLH
vll
reproduction time [days]
high
low
high
low
high
low
N = 119
Fig. 7 The impact of feeding levels during development and reproduction on bridge spider
lifespan. The time bar is rooted (time = 0 days) at maturation; development time has a negative
sign. Lifespan of bridge spiders increases with decreasing food availability. Limited food during
development shifts the ratio between development time and reproduction time towards
development time, however, limited food after maturation leads to longer reproductions periods.
Discussion
Lifetime fecundity and lifespan of the bridge spider Larinioides sclopetarius is under the
influence of feeding during growth and reproductive period. Spiders that were exposed to
high prey availability throughout their entire life produced four times more offspring
despite living half as long as spiders with poor prey availability. However, spiders with
limited food throughout their juvenile and adult life partly compensated for the resulting
disadvantages in growth and reproductive rates by increasing developmental and
reproductive time.
Impact of food availability during developmental period on lifetime fecundity
The impact of food availability during development on lifetime fecundity in bridge spiders
is mediated by the effects of different feeding conditions on the life history traits, size and
age at maturation (see Chapter 2). However, the nature of the interactions between prey
availability during development, fecundity, and life history traits remains cryptic. We
assume that the influence of the juvenile feeding treatment on lifetime fecundity is caused
by its effects on age, rather than size, at maturity. Among the three life history parameters
80
DIETARY RESTRICTION INCREASES LIFETIME FECUNDITY AND EXTENDS LIFESPAN
CHAPTER 3
examined in Chapter 2 feeding condition and lifetime fecundity are only related to age at
maturity: females under limited food mature at an older age, which reduces lifetime
fecundity. An increase in size at maturity increases the fecundity in female bridge spiders
but we found no direct relation between size at maturity and juvenile feeding conditions
in Chapter 2. In contrast, the weight at maturity, while significantly correlated to feeding
level (Chapter 2) showed no significant link to lifetime fecundity, although we found a
tendency for increasing offspring number with increasing female weight.
Our data suggest a life history trade-off in bridge spiders between size and age at
maturity with fecundity (Roff 1992, Stearns 1992). Size at maturity is canalized suggesting
that bridge spiders optimize their adult size at the cost of a prolonged developmental time
(Chapter 2). The positive relation between size at maturity and female fecundity, and the
negative relation between age at maturity and fecundity found in this study are in
accordance with our previous hypothesis of an optimized female size (Chapter 2). The
increase in fecundity of larger females is counterbalanced by a decrease in the number of
egg sacs and eggs in spiders that mature at an older age. Thus we present experimental
evidence in the bridge spider for the life history trade-off between size and age at maturity,
which effects lifetime fecundity (Roff 1992, Stearns 1992).
The trade-off between size and age at maturity was often used to predict the body size
of animals (i.e. the equilibrium model for body size, Arak 1988, Schluter et al. 1991,
Fairbairn 1997, Blanckenhorn 2000, 2005). For females, the positive effect of size on
fecundity is contrasted by the higher risk of mortality over a longer developmental period
due to predation, parasitism, and starvation. In our laboratory experiment, extrinsic
mortality costs on juvenile bridge spiders were absent implying that the negative effect of
age at maturity on lifetime fecundity was caused by intrinsic factors. We suggest that those
intrinsic factors were physiological costs that might be related to senescence.
Numerous studies have demonstrated positive effects of female body size on fecundity
(Petersen 1950, Kessler 1971, Beck and Connor 1992, Head 1995, Spence et al. 1996, Brown
et al. 2003, Hendrickx and Maelfait 2003, Walker et al. 2003, Foellmer and Moya-Laraño
2007). The increase in female fecundity can be due to an increase (1) in the number of eggs
per clutch or (2) in the number of clutches. Bridge spiders increase their fecundity through
an increase in the number of eggs per clutch because the number of egg sacs is not
81
CHAPTER 3
DIETARY RESTRICTION INCREASES LIFETIME FECUNDITY AND EXTENDS LIFESPAN
influenced by the size at maturity. Rather, the number of egg sac a female can produce is
limited by the time available for reproduction.
Although a prolonged development time decreases the number of egg sacs, bridge
spiders generally produce more clutches (on average 6.0 egg sacs, up to 15) than most
other spider species (1-2 clutches, reviewed by Marshall and Gittleman 1994). There are
only a few spider species that produce more than three clutches and usually an increased
number of clutches is combined with a reduction in clutch size (Marshall and Gittleman
1994). Bridge spiders have a mean clutch size of 76.7 eggs, which fits well into the range of
spider species with one or two egg sacs. The American house spider Parasteatoda
tepidariorum produce an exceptionally high number of clutches (9.7) combined with a
comparatively large clutch sizes (186.9 eggs) (Miyashita 1987). Like L. sclopetarius, P.
tepidariorum is a successful cosmopolitan and synanthropic species (Levi 1967) and it can
overwinter in juvenile and adult stages (Tanaka 1991). Non-seasonality in bridge and
house spiders might be related to their anthropogenic habitats and was previously
discussed as a general characteristic of urban species (Chapter 1).
Impact of food availability during reproductive period on lifetime fecundity and egg weight
High prey availability during the reproductive period is directly converted into lifetime
fecundity by increasing clutch size and shortening the intervals between clutches. The
positive correlation between food availability and reproductive success is a widespread
phenomenon in arthropods (Wise 1979, Fritz and Morse 1985, Sota 1985, Pékar 2000,
Allard and Yeargan 2005). The increase in clutch sizes and the shortening of intervals
between consecutive clutches allows bridge spiders to immediately respond to high prey
densities by increasing reproductive output. Trap building spiders frequently encounter
variable prey densities and are generally thought of as being food limited (Wise 1979,
Mayntz et al. 2003). There is general agreement that the possibility for spiders to respond
to high food availability by immediately increasing their reproductive output evolved as an
adaptation to temporal fluctuations in prey abundance (Anderson 1970, Wise 1979).
An unexpected result was that the mean egg weight was affected by whether the egg
was fertilized or not. What makes fertilized eggs heavier than unfertilized eggs? There
might be two reasons for this: (1) cryptic resource allocation of females and (2) processing
of eggs after fertilization and deposition. Cryptic resource allocation between copulation
82
DIETARY RESTRICTION INCREASES LIFETIME FECUNDITY AND EXTENDS LIFESPAN
CHAPTER 3
and oviposition could be due to an egg provisioning mechanism that is directly coupled to
fertilization. Bridge spiders produce egg sacs even when they are un-mated or their sperm
reserves are depleted (pers. observation). It is conceivable that spiders with empty sperm
stores invest fewer resources in egg sacs than spiders with sufficient sperm. This requires a
mechanism for the female to measure sperm in storage and it raises the question why
unfertilized clutches are produced to begin with. In addition, cryptic resource allocation
can only explains differences between egg sacs that are 0 or 100 percent fertilized, but it
cannot explain the gradual weight decrease of egg sacs that are fertilized to a lower
degree than 100 percent.
The processing of eggs after fertilization may include chemical modifications that
increase the hygroscopic character of fertilized eggs or that prevent fertilized eggs from
drying out. Weight differences would then be due to differences in the amount of water.
After oviposition, the egg mass hardens (pers. observation, Foelix 1996). In fish eggs,
hardening increases the weight of fertilized eggs due to water influx (Lahnsteiner et al.
2001, Lahnsteiner and Patzner 2002). Although the mechanism remains unknown we
propose a similar connection between egg hardening and egg weight increase in spiders.
The reproductive allocation patterns of L. sclopetarius are clearly shaped by the trade-off
between clutch size and egg weight (i.e. between number and size of offspring). This
trade-off was also found in the wolf spider Pirata piraticus (Lycosidae) (Hendrickx and
Maelfait 2003) but not in the wolf spider Hogna helluo (Lycosidae), the pholcid spider
Holocnemus pluchei (Pholcidae), and the crab spider Misumena vatia (Thomisidae) (Fritz
and Morse 1985, Skow and Jakob 2003, Walker et al. 2003). The decrease in egg weight
within larger clutches is independent of the feeding level because egg weights at different
feeding levels were not significantly different. This suggests that feeding condition of the
female does not affect the quality of eggs but the quantity. Thus, the trade-off between
egg weight and egg number cannot be compensated for by larger amounts of food.
Kessler (1971) and Wise (1979) also found no influence of the amount of food on egg
weight in spiders.
Dietary restriction, lifespan, and fecundity
The effects of feeding conditions on life span and on the relative durations of development
and reproduction are complex. High feeding conditions during the entire life of female
83
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DIETARY RESTRICTION INCREASES LIFETIME FECUNDITY AND EXTENDS LIFESPAN
bridge spiders resulted in a shorter development time and in shorter intervals between
clutches after maturation. Reproduction time increased in spiders with high feeding
conditions during growth but decreased with high feeding conditions after maturation.
Lifespan is shortest in spiders that experienced high prey abundances over the entire life.
Bridge spiders with limited food can compensate for temporal factors like intervals
between clutches by prolonging lifespan. Thus, they produced the same number of
clutches but they cannot increase the number of eggs per clutch.
The extension of life by dietary restriction in animals is a widespread phenomenon (for
review see Masoro 2005). There are several hypotheses ranging from growth and
metabolism to molecular processes to explain this pattern. However, the underlying
biological mechanism for longevity under dietary or caloric restriction is still not known.
Among the possible mechanisms that Masoro (2005) discussed, the retardation of growth
hypothesis (lower growth under caloric restriction) and the reduction of metabolic rate
hypothesis (lower metabolism under caloric restriction) are best applicable to bridge
spiders.
Retardation of growth in L. sclopetarius was previously demonstrated in Chapter 1;
growth rates under limited food were significantly lower than under unlimited food. The
retardation of growth hypothesis, however, cannot explain the prolonged lifespan for
spiders that grew under ad libitum conditions but had limited food after maturation.
Reduction of metabolic rate could slow down senescence in spiders because their
metabolism is generally low compared to other ectothermal animals of similar size
(Anderson 1970), and spiders can reduce their metabolism at hibernation (Foelix 1996).
The low metabolic rates were proposed to be correlated with the periods of starvation
frequently encountered by spiders (Anderson 1970). Although measurements of metabolic
rates were beyond the scope of this paper, the responses in life history and reproductive
parameters to limited food observed in this study and in Chapter 1 and 2, suggest that
bridge spiders are able to down regulate their metabolic rates in periods of limited prey
abundance.
In this study we investigated the link between longevity and fecundity and we found an
inverse relationship between reproduction and survival. Similar results were found in a
study on the bowl and doily spider Frontinella pyramitela (Austad 1989). In spiders, the
costs of longevity are decreased lifetime fecundity and a higher extrinsic mortality risk due
84
DIETARY RESTRICTION INCREASES LIFETIME FECUNDITY AND EXTENDS LIFESPAN
CHAPTER 3
to longer development and reproduction time. Consequently, natural selection will favor
spiders that increase their food intake at the cost of longevity if that raises fecundity. This
might also explain why some spider species gorge food even though this behaviour results
in greater mortality (Higgins and Rankin 2001, Marczak and Richardson 2008).
Conclusion
As expected, female L. sclopetarius that are exposed to high prey abundances exhibit
higher numbers of offspring (many clutches with lots of eggs) during a short lifespan;
dietary restrictions slow down senescence and cause an extended lifespan. The increase in
reproductive output as response to high prey abundances makes bridge spiders very
successful in colonizing new habitats. Surprisingly, the quality of eggs (egg weight) is
independent of the feeding conditions females encounter during their lives. Although
food availability was found to have no impact on female size (Chapter 2), size at maturity is
positively correlated with lifetime fecundity. However, despite having similar size, females
that grew under poor diet had lower fecundity and shortened reproductive periods due to
longer development, which results in the predicted trade-off between size and age at
maturity.
Food availability during developmental and reproductive period affected lifetime
fecundity. However, the mechanisms determining how food alters fecundity differ
between life stages. Juvenile feeding treatments influenced the reproductive output by
changing the life history traits, especially the age at maturity; adult feeding treatment
influenced the rate of egg deposition by decreasing intervals between clutches. The effects
of feeding treatments on different life history stages can be: (1) equal (e.g. better feeding
condition in juveniles and adults will increase fecundity), (2) counteracting (e.g.
reproductive time is prolonged if a rich diet is received during development but shortened
if it is received after maturation), or (3) one-sided (e.g. intervals between clutches are only
affected by adult feeding treatment and not by juvenile feeding treatment). These
complex interactions demonstrate the necessity to consider an organism’s life stages when
examining environmental impacts on life history.
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DIETARY RESTRICTION INCREASES LIFETIME FECUNDITY AND EXTENDS LIFESPAN
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General discussion
The complexity of life history research
Life history strategies of organisms are very complex; different selection pressures and
trade-offs between life history traits act during different life stages (Roff 1992, Stearns
1992). Thus, life stages should be considered separately but also concertedly to identify the
extrinsic and intrinsic selection pressures and trade-offs that shaped life histories. The
ability to respond to extrinsic factors, such variation in food availability should be
expressed in an organism’s life history traits and the most suitable models to target are
invasive colonizers that rapidly expand into novel environments. The bridge spider
Larinioides sclopetarius is a very successful colonizer of urban habitats that has the
potential to expand exponentially. With bridge spiders as model organism, I investigated
how life histories are shaped under varying selection pressures and trade-offs at different
stages of life.
Life history strategies of laboratory reared bridge spiders
The first life stage – the developmental period – of bridge spiders is characterized by high
developmental plasticity (Chapter 1). All developmental parameters such as the number of
instars, the interval between instars, and the growth rate were affected by food availability
in males and females. Growth of bridge spiders followed a geometric progression that
unlike Dyar’s rule (Dyar 1890, Przibram and Megušar 1912) has non-constant growth ratios
between successive instars. Poor diet delayed growth by adding additional molts to reach
larger sizes at maturity, which causes older ages at maturity (trade-off between age and
size at maturity, Chapter 2). Nevertheless, females even aligned their body sizes
irrespective of feeding conditions, suggesting that female body size is under stabilizing
selection. Males became larger with increased food availability suggesting that their body
size is affected by directional selection. The result that female size is canalized while male
size showed higher variability is in accordance with Rensch’s rule (Rensch 1950, Fairbairn
and Preziosi 1994, Fairbairn 1997, Blanckenhorn et al. 2007).
The second life stage – the reproductive period – is characterized by female variability in
reproductive output (Chapter 3). Females under rich diet during reproduction were able to
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produce high numbers of offspring in a short time (short egg sac deposition intervals). The
offspring quality (egg weight) was not influenced by food availability but it decreases with
increasing clutch size (trade-off between number and size of offspring). Poor diet caused
delayed senescence and thus a longer reproductive period but also a decrease in lifetime
fecundity.
So how can we combine these results to compare different trade-offs and selection
pressures on distinct life stages? Feeding conditions during developmental and
reproductive period have an impact on lifetime fecundity. However, there are four possible
combinations on how diet influences lifetime fecundity in the experiment presented here.
First, a rich diet at both life stages results in high numbers of offspring during a short life
and thus the highest lifetime fecundity in the experiment. Second, poor diet throughout
life extends lifespan but results in the lowest lifetime fecundity. Third, spiders that grew
under poor diet but had unlimited food after maturation, compensated for their slower
growth by having short intervals between clutches and by producing relatively high
offspring numbers. Fourth, spiders that grew under unlimited feeding conditions but
encountered a restricted diet during reproduction had a lifetime fecundity that was almost
as low as in spiders with poor diet throughout life.
Although diet during development and reproduction altered lifetime fecundity, the
effects of feeding conditions after maturation had a greater impact on reproductive
success than diet during growth. Disadvantages caused by food limitations during
development were almost compensated for by unlimited food after maturation while in
contrast, poor diet during reproduction always resulted in lower fecundity, even in
individuals that were well-fed during growth. Despite these unambiguous laboratory
results, we have to interpret them according to the natural food environment bridge
spiders experience in their natural environment. Thus, the results from this laboratory
based thesis can then be applied to interpret the ecological success of L. sclopetarius in
cities.
The ecological success of bridge spiders
The life history response to diet in bridge spiders is likely to be linked to local conditions in
prey abundance. These spiders feed almost exclusively on chironomids that hatch from
nearby water. I suggest that the timing of reproduction in bridge spiders in the field will
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GENERAL DISCUSSION
coincide with periods of high prey abundance and thus should overlap with the seasonal
emergence of chironomid larvae from water (spring, summer, and fall species, Ziegler
2005). Seasonal mass emergence is a common anti-predation strategy of many prey
species (Ims 1990) and predators may have difficulties to adapt their life history traits to
such conditions. The enormous flexibility in reproductive allocation and the high tolerance
to low food availability, however, enables bridge spiders to survive and flourish under such
conditions. While mass emergence events will limit reproduction to single or few peaks per
season in a natural environment, illumination of cities provide food at all time by attracting
additional insects from surrounding areas (Eisenbeis and Hassel 2000) and thus prolong
the season and as a result the spiders become overabundant.
Food availability throughout life directly affected the lifetime fecundity of females and
had a direct impact on current resource allocations. This rapid proliferation allows these
spiders to become locally dominant in a short time period, which is characteristic for
invasive species in general (Richardson et al. 2000, Kolar and Lodge 2001, Colautti and
MacIsaac 2004). For example, in plants invasiveness is related to early flowering, high initial
growth rate, and high reproductive output (Garcia-Serrano et al. 2005). Although a
comparison of plants and spiders is of limited utility, there are some interesting parallels: (i)
the young age at maturity in bridge spiders under high food (Chapter 2) is analogous to
early flowering in plants, (ii) high initial growth rate in plants is similar to the rapid
potential growth in bridge spiders (Chapter 1), and (iii) invasive plants and bridge spiders
share a high reproductive output (Chapter 3).
Costs of rapid growth can be an increased mortality risk, which relates to molting
problems that other spiders under unlimited food encounter (Higgins and Rankin 2001,
Marczak and Richardson 2008). Unlike other spiders, in bridge spiders variation in growth
and reproductive allocation did not influence mortality and bridge spider mortality is not
increased at high feeding level. Conversely, even under extremely limited food availability,
mortality was not affected by the laboratory experiment (Chapter 1) and because of the
spatially and temporally limited presence of only a few predators feeding on bridge
spiders (e.g. sparrows, tits, pers. observation), I do not expect a high extrinsic mortality in
urban habitats. This suggests that life-history plasticity is not limited by intrinsic or extrinsic
mortality. Further, bridge spiders can produce offspring also during periods of food
limitation (Chapter 3).
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GENERAL DISCUSSION
LIFE HISTORY OF THE BRIDGE SPIDER
With high food availability, female bridge spiders can produce up to 15 clutches per
lifetime (Chapter 3). The production of several clutches (iteroparity) rather than investing
in a single or few reproductive events (semelparity) is expected when adult mortality is low
(Young 1990, Stearns 1992), a prediction that is supported by this study on L. sclopetarius.
Indeed, the reproductive period of the bridge spider can exceed its developmental time
(Chapter 3). Unlike most other spiders, including the coexisting species Zygiella x-notata,
which produce maximally three clutches (Marshall and Gittleman 1994, Wherry and
Elwood 2009) or species in which only one cocoon is laid (Fritz and Morse 1985, Beck and
Connor 1992, Schneider and Lubin 1997, Salomon et al. 2005), L. sclopetarius immediately
converts resources into eggs over an extended time period and will not only adapt clutch
size to current conditions but can also modify intervals between clutches. The consecutive
deposition of clutches in bridge spiders allows for rapid adjustment of reproductive effort
to current prey availabilities throughout the year.
Bridge spiders do not show pronounced seasonality as all life stages are present
throughout the year including mature males and females (except for egg sacs that do not
overwinter) (Nioduschewski and Kraayvanger 2005, Schmitt and Nioduschewski 2007) The
almost perpetual presence of spiderlings and egg sacs of bridge spiders is relevant for pest
control in urban habitats, because cleaning of artificial facilities will only have a short term
effect on their population densities.
The high population densities that bridge spiders can achieve and that resulted in their
reputation as pest in cities with waterfronts are also favored by an unusual tolerance
between conspecifics. Bridge spiders were previously considered parasocial (Schmitt 2004,
Nioduschewski and Kraayvanger 2005), because they aggregate in loose communities with
shared usage of retreats (Foelix 1996). The tolerance and reduced territoriality of bridge
spiders likely result from the high resource availability (prey, space, retreats) in urban
habitats.
Conclusion and outlook
Herein, I demonstrated a remarkably high flexibility in life history traits of bridge spiders at
different life stages. Except for female size at maturity and offspring size (egg weight), all
parameters that define a spider lifecycle are influenced by variable diet regimes. I
suggested that bridge spiders are adapted to extreme fluctuations in prey abundance as is
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LIFE HISTORY OF THE BRIDGE SPIDER
GENERAL DISCUSSION
characteristic for mass emerging insects in their natural environment. In this study I did not
simulate such extreme fluctuations but kept food availability constant within the two life
stages (development and reproduction), but at different levels (high and low). Hence,
conclusions about the adaptive significance of developmental and reproductive plasticity
are only indirect. Further experiments on life histories under variable environmental
factors should also alter diet within life stages, for example by varying developmental food
supply after molts or by changing food amount at reproduction after the deposition of the
first clutch.
To conclude on the conditions that spiders encounter in urban habitats it will be
important for future studies to compare the life history traits of the laboratory reared
spiders with spiders in the field. Differences in life history traits between field and
laboratory populations could be due to differences in food quantity but also quality. Field
experiments should thus also determine prey densities and prey composition. Further, the
impact of food quality should also be assessed by an experiment that alters the nutritional
intake at identical prey amounts (Toft and Wise 1999, Mayntz et al. 2003, Rickers et al. 2006,
Wilder and Rypstra 2008, Kolss et al. 2009).
Bridge spiders are successful in invading urban habitats because they can exploit
artificial structures (bridges, facades, artificial light sources) and high insect abundances
that are attracted by light at night. However, there is a lack of data on rural (non-urban)
bridge spider populations. A comparison between life histories of urban and rural bridge
spider populations will enhance our knowledge on the characteristics of species that have
the potential to become invasive in urban habitats and thus will contribute to our current
understanding of urban ecology.
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GENERAL DISCUSSION
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Danksagung
Prof. Dr. Jutta M. Schneider gilt mein besonderer Dank dafür, dass sie mir das
Brückenspinnen-Projekt anvertraut und mich damit auch in die schöne Stadt Hamburg
geholt hat, sich immer um mich gekümmert hat und um meine Finanzierung besorgt war,
sie stets für Fragen und Diskussionen zur Verfügung stand, mir den schnellen Endspurt
ermöglicht hat und dadurch insgesamt eine ganz tolle Betreuerin war.
Prof. Dr. Marie E. Herberstein danke ich für die äußerst wertvollen Kommentare und die
konstruktive Kritik für den schriftlichen Teil meiner Arbeit, ebenso für den 'Morning tea',
der so manchen dunklen Herbsttag erhellen konnte.
Den Mitarbeitern der Abteilung Verhaltensbiologie der Universität Hamburg danke ich
insgesamt für eine super Arbeitsatmosphäre und nette Mensa- und Kickerrunden. Dr. Lutz
Fromhage danke ich für die wertvollen Diskussionen, Verbesserungsvorschläge und
sprachlichen Tipps; Helma Roggenbuck, Nicole Ruppel und Klaas Welke (in alphabetischer
Reihenfolge) dafür, dass sie immer ein offenes Ohr für mich hatten, mit mir diskutiert
haben, Abbildungen angesehen und englische Vokabeln jongliert haben. Unseren beiden
höchst engagierten technischen Angestellten Tomma Dirks und Angelika Taebel-Hellwig
danke ich für die Versorgung der Brückenspinnen in Zeiten, in denen ich nicht anwesend
war, dafür, dass sie das Labor und die Abteilung immer in Schwung gehalten haben, sich
sowohl um mein leibliches als auch um mein seelisches Wohl gekümmert haben. Dr. Ralf
Wanker danke ich für seine Hilfe bei statistischen Fragen. Unserem Tischlermeister Ralph
Mistera und Mechaniker Mario Märzke (alias Super-Mario) danke ich dafür, dass sie für das
Projekt benötigte Phantasiegebilde handwerklich immer einwandfrei und schnell
zusammengebaut haben.
Dr. Mason N. Dean danke ich für das sehr gewissenhafte Überprüfen und Korrigieren der
englischen Sprache dieser Arbeit.
Der HafenCity Hamburg GmbH, mit ihrem Geschäftsführer Jürgen Bruns-Berentelg, und
weiteren Investoren danke ich für die Finanzierung des Projektes und meiner Doktorarbeit.
Der Assistentin der Geschäftsführung der HafenCity Hamburg GmbH Bianca Penzlien
danke ich für die gute Zusammenarbeit.
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DANKSAGUNG
LIFE HISTORY OF THE BRIDGE SPIDER
Meiner Mutter, Gisela Kopmann, danke ich dafür, dass sie mich immer unterstützt und
besucht hat und zu jeder Zeit ein offenes Ohr für mich hatte.
Zuletzt aber ganz besonders danke ich meinem lieben Ehemann, Dr. Thomas Kleinteich,
ohne den ich diese Arbeit niemals hätte so zustande bringen können. Ich danke ihm für
seine unendlich große Hilfe bei der englischen Übersetzung, die vielen Stunden der
Diskussion, den guten Ideen und dafür, dass er immer für mich da war und mich in meiner
Doktorandenzeit in Hamburg erobert hat. Du bist das Beste, was mir je passiert ist!
100